biodegradative and biosynthetic capacities of mushrooms: present and future strategies

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91

Critical Reviews in Biotechnology, 18(2&3):91–236 (1998)

Biodegradative and Biosynthetic Capacities ofMushrooms: Present and Future Strategies

Somasundaram Rajarathnam,* Mysore Nanjara jaUrs Shashirekha,and Zakia BanoFruit and Vegetable Technology, Central Food Technological Research Institute, Mysore – 570013India

* Corresponding author.

TABLE OF CONTENTS

I. INTRODUCTION ....................................................................................................... 92

II. MORPHOLOGY AND LIFE CYCLE ..................................................................... 93

III. CHEMISTRY AND NUTRITIONAL EVALUATION .......................................... 93

IV. BIODEGRADATIVE CAPACITIES ........................................................................ 97A. Degradation of Cellulose, Hemicellulose, and Lignin ............................................ 98B. Mechanism of Lignin Degradation ........................................................................ 102C. Degradatory Enzymes ............................................................................................ 106D. Ligninolytic Enzymes ............................................................................................ 108

1. Lignin Peroxidases ........................................................................................... 1082. Manganese Peroxidases.................................................................................... 1093. Laccases ............................................................................................................ 1104. Aryl-alcohol Oxidases ...................................................................................... 110

E. Biological Pulping .................................................................................................. 112F. Kraft Pulp Discoloration ........................................................................................ 114G. Decolorization of Waste Waters ............................................................................ 116H. Coal Solubilization ................................................................................................. 118I. Degradation of Polystyrenes .................................................................................. 119J. Bioremediation of Toxic Environmental Pollutants .............................................. 119

1. Chlorinated Organic Compounds..................................................................... 1192. Polycyclic Aromatic Hydrocarbons ................................................................. 1213. Nitro-substituted Compounds .......................................................................... 1224. Dyes .................................................................................................................. 1235. Other Toxic Compounds .................................................................................. 123

V. BIOSYNTHETIC CAPACITIES ............................................................................ 124A. Biomass .................................................................................................................. 124B. Carbohydrates ......................................................................................................... 126

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C. Amino Acids, Peptides, and Proteins .................................................................... 129D. Lipids ...................................................................................................................... 137E. Vitamins ................................................................................................................. 139F. Flavor Component .................................................................................................. 141G. Nucleic Acids ......................................................................................................... 145H. Minerals .................................................................................................................. 145I. Pigments ................................................................................................................. 151J. Chitin ...................................................................................................................... 151K. Polysaccharides ...................................................................................................... 152L. Other Biological Useful Constituents .................................................................... 157M. Toxic Substances .................................................................................................... 159N. Enzymes and Co-enzymes ..................................................................................... 164

1. Carbohydrases .................................................................................................. 1642. Proteinases ........................................................................................................ 1663. Lignin-Peroxidases and Manganese-Peroxidases ............................................ 1664. Phenol-Oxidases ............................................................................................... 1685. Oxido-Reductases and Pyranose-Oxidases ...................................................... 1736. Other Enzymes ................................................................................................. 173

O. Various Other Compounds..................................................................................... 175

VI. BIOLOGICAL ODDITIES ...................................................................................... 179

VII. CONCLUSIONS ........................................................................................................ 182

ACKNOWLEDGMENTS ......................................................................................... 186

REFERENCES .......................................................................................................... 186

I. INTRODUCTION

As a group of highly specialized fungi,mushrooms are known for a number of proper-ties — biological, chemical and biochemical.In nature, about 2000 edible species areknown, of which 80 are grown experimentallyand around 22 cultivated commercially(Rajarathnam et al., 1992; Chang et al., 1993).In nature, they grow on soil or wood. Theyhave varied requirements of nutritional andenvironmental conditions. They may be tropi-cal, subtropical or temperate and accordingly,they enjoy a worldwide distribution; also sev-eral species occur in different seasons in thesame region (Chang and Hayes, 1978;Rajarathnam and Zakia Bano, 1991). They havetwo phases in their life cycle viz., the mycelium(vegetative phase) that lasts longer in the lifecycle and the fruiting body (reproductive phase)

that bears the spores. The mycelium growsthrough the substrate, biodegrades the substrateand supports the formation of fruiting bodies.While the growth of mycelium lasts for severaldays, weeks or months; production of fruitingbodies is short lived, a few days, and the phe-nomenon is called ‘fructification’. The appar-ent biomass that can be harvested free of sub-strate, in the form of fruiting bodies merits theusefulness of such culturing of mushrooms insolid state fermentation. This reflects on thefast rate of metabolic activity during fructifica-tion. Obviously, this is a system channelizingthe nutrients derived from the substrate andcontained in the mycelium to the developingfruiting bodies. They are also items of “fooddelicacy” because of their characteristic bitingtexture and flavor. The capacities and capabili-ties of mycelium to biodegrade the substrateare enormous and multitudinal. On the other

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hand, the chemical, biological, and biochemi-cal properties of the fruiting bodies are numer-ous. In this review, efforts are made to give aconcerted picture of the “degradative”, aswell as “constructive” capacities of the mush-rooms.

II. MORPHOLOGY AND LIFE CYCLE

In nature, mushrooms represent the con-spicuous structures of mycelial construction,of varied shape, size, color, texture and struc-ture, with a primary function to bear and dis-seminate the spores, for the perpetuation of thespecies. The mycelium is mostly inconspicu-ous, hidden in the growth substrate which ex-presses as tiny fruiting primordia (with the onsetof favorable conditions), which ultimately growinto the fruiting bodies. Spore to spore stagewhich is defined as the “life cycle” is ratherelaborate and at times complicated too, withthe highly evolved basidiomacromycetes(Rajarathnam et al., 1992). A typical life cycleis illustrated (Figure 1) of a typical tetrapolarspecies (Rajarathnam and Zakia Bano, 1987,Chang et al., 1993). Here the spore germinatesto produce the mycelium and the monokaryoticmycelium of monosporous origin, is requiredto become dikaryotic to produce and bear thebasidiospores. The compatible monokaryonsby pairing, result in dikaryons, which by virtueof their nuclear contents have a stronger capac-ity to grow, secrete enzymes and biodegradethe growth substrate(s), which in turn aid thebuild up of the vegetative mycelium. Under theideal conditions of temperature, humidity,growth factors, etc., the mycelium resorts tothe production of fruiting initials, followed bythe differentiation of basidia, to bear the basid-iospores; each basidium to bear 4 types of ge-netically different spores (tetrapolar), so thatthe extent of in-breeding is reduced to 25%,with a vast scope for out-breeding and thus, agreater chance to generate variants. The extentof variability is compounded by the multiplealleles at different loci, which in turn target tobuild up higher and higher degrees of variabil-

ity (Chandrashekar et al., 1981; Chang et al.,1993).

A great amount of research interest is vestedin the study of the patterns of sexuality of thebasidiomacromycetes. This study is of para-mount importance while exploiting the ediblespecies for the production of flavored fruitingbodies for human consumption. The sexualitycan be as simple as primary homothallism, asin Volvariella volvacea; secondarily homothal-lic as in Agaricus bisporus; heterothallic andbipolar as in Agaricus bitorquis, Pholiotanameko, and Auricularia auricula; or heteroth-allic and tetrapolar as in Auricularia polytricha,Lentinus edodes, Flammulina velutipes,Pleurotus ostreatus, Pleurotus flabelatus, andCoprinus fimetarius (Raper, 1978, Miles, 1993).

III. CHEMISTRY AND NUTRITIONALEVALUATION

Fresh mushrooms in general contain about90% moisture, the rest accounting for the drymatter. In order to ensure universal comparisonof chemical analytical data of various mush-room species reported from different parts ofthe world, the chemical constituents are ex-pressed on a dry weight basis. Carbohydratesaccount for approximately 60%, proteins 25%,fat 5% and the remaining 10% is representedby ash (Table 1), which includes various min-erals.

The energy value of a food can be esti-mated based on its content of crude protein, fatand carbohydrate, using the Atwater factors of4.0, 9.10 and 4.2 KCal g–1 of each component,respectively (FAO, 1973). In mushrooms, how-ever, these components are not 100% digest-ible and conversion factors of 2.62, 8.37 and3.48 are usually used to correct for the reduceddigestibility of protein 70%; fat 90%; and car-bohydrate 85% (Crisan and Sands, 1978).Obviously mushrooms are low-calorie foodsand if included in the daily diet in a proper dosewould be helpful in reducing obesity. Thesubject of chemical composition of mushroomsis reviewed by several authors (Crisan and

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FIG

UR

E 1

.D

iagr

amm

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of a

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tet

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mus

hroo

m s

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(Ada

pted

fro

m R

ajar

athn

am a

nd Z

akia

Ban

o, 1

987a

.)

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Sands, 1978; Zakia Bano and Rajarathnam,1982, 1988; Rajarathnam and Zakia Bano, 1991;Rajarathnam et al., 1992b, Buswell and Chang,1993). Dietary fiber is a prominent componentof mushrooms. Kurasawa et al. (1991) deter-mined the content in 47 species of mushroomsby the enzymatic/gravimetric method and in-volvement of chitin correction. Several refer-ences have documented the data of mushrooms;their constituent carbohydrates, amino acids,proteins, fat, vitamins, and nucleic acids(Sotomko et al., 1987; Kochetova et al., 1988;Abou-Helilah et al., 1987; Senatore et al., 1988;He et al., 1988; Bakowski and Kosson, 1985;Stancher et al., 1990; Lassek and Montag, 1990;Horie et al., 1991; Blanco et al., 1992; Yoshidaand Hoshino, 1992). Details of each ofthe major components are dealt within Sec-tion V.

Quantitative data relating to the nutritivevalue of mushrooms are sparse. In the absenceof animal feeding trials, several other methodshave been used for determining or predicting

the nutritional value of foods based on theircontent of essential amino acids (Table 2)(Crisan and Sands, 1978). The chemical scoreis based on the amount of the most limitingamino acid present in the test protein relative tothe amount of that particular amino acid in thereference protein (egg) and is calculated usingthe formula,

Chemical Score =g essential amino acid in test protein

total essential amino acids in test protein

total essential amino acids in egg

g essential amino acids in egg× × 100

The chemical score reflects the “percent-age adequacy” of the protein and approximatesthe probable efficiency of the test protein inchildren. By calculating a factor, equal to 100times the reciprocals of the amino acid score,one can determine the quantity of the test pro-tein required to provide the minimal aminoacid pattern present in the reference

TABLE 1Approximate Composition a of Fruiting Bodies of Basidiomycetes

Crudeprotein Carbohydrate

Species (N ××××× 4.38) Fat value (Kcal) Fiber Ash Energy

Agaricus bisporus 26.3 1.8 59.9 10.4 12.0 328Auricularia auricula-udae 8.1 1.5 81.0 6.9 9.4 356Auricularia polytricha 7.7 0.8 87.6 14.5 3.9 347Boletus edulis 29.7 3.1 59.7 8.0 7.5 362Cantharellus cibarius 21.5 5.0 64.9 11.2 8.6 353Collybia albuminosa 26.6 4.0 67.5 8.1 7.0 365Coprinus comatus 25.4 3.3 58.8 7.3 12.5 366Flammulina velutipes 17.6 1.9 73.1 3.7 7.4 378Lentinus edodes 17.5 8.0 67.5 8.0 7.0 387Lycoperdon lilacinum 46.0 7.5 38.8 12.3 7.7 358Pholiota nameko 20.8 4.2 66.7 6.3 8.3 372Pleurotus florida 18.9 1.7 58.0 11.5 9.3 265Pleurotus eous 17.5 1.0 59.2 12.0 9.1 261Pleurotus limpedus 38.7 9.4 46.6 27.6 5.3 313Termitomyces microcarpus 27.4 4.3 54.2 2.2 14.1 364Tricholoma species 16.7 3.1 71.9 12.9 8.3 342Volvariella esculenta 34.4 20.6 31.7 11.2 13.3 396

a On dry weight basis.

Adapted from Rajarathnam et al., 1992b.

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TABLE 2Estimated Nutritive Value of Mushroom Species

Essential amino Biological Nutritional Amino acidSpecies acid index value index score a

Agaricus bisporus 55.8 49.1 17.0 36Boletus edulis 76.6 71.8 0.3 37Cantharellus cibarius 86.2 82.3 3.0 68Lentinus edodes 55.8 49.1 9.8 40Pholiota mutabilis 85.5 81.5 N.A.b 67Pleurotus eous 95.7 92.7 16.7 59Pleurotus florida 84.5 80.4 5.9 67Pleurotus flabellatus 82.7 78.4 17.8 47Pleurotus sajor-caju 70.9 59.2 14.4 67Pleurotus ostreatus 64.8 58.9 13.6 40Russula vesca 88.9 85.2 6.0 70Termitomyces microcarpus 74.7 69.7 20.5 45Volvariella displasia 87.9 84.1 25.1 71

a Using egg as reference protein.b Not available.

Adapted from Rajarathnam et al., 1992b.

protein. The amino acid score is calculated asfollows:

Amino acid score =mg of amino acid in one g test protein

mg of amino acid in one g reference protein× 100

It indicates the most limiting amino acid inthe food protein.

Essential amino acid index (EAA index)was proposed by Oser (1959) to evaluate thequality of dietary protein in terms of the ratioof the essential amino acids contained in afood, relative to the essential amino acid con-tent of a highly nutritive reference protein.Whole egg protein is used as the referenceprotein.

EAA

n

index* =Lysine Tryptophan Histidine

Lysine Tryptophan Histidine

number of amino acids

p = food protein

s = standard (egg)

p p p

s s s

n

* =

The EAA index is used to predict the BiologicalValue (BV) of the food, a measure of the nitro-gen retained by the body after consuming thetest protein. It is predicted that BV approximatesthe BV obtained in animal feeding studies.

Biological Value = 10.9 (EAA Index) –11.7

In an attempt to resolve the difficulties in-herent in comparisons between those mush-rooms containing small amounts of high qual-ity protein with those containing larger amountsof a protein of lesser nutritional qualities, thenutritional index is calculated (Crisan andSands, 1978):

Nutritional Index =(EAA index percentage protein)

100

×

According to Crisan and Sands (1978), themost nutritive mushrooms, which have a highEAA index and amino acid score are almostequal in nutritional value to meats and milk,whereas the mushrooms showing the least nu-tritive value, rank considerably lower but are

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comparable to vegetables like carrots and to-matoes. When the nutritional index is takeninto consideration, the mushrooms rank aboveall vegetables and legumes. Hence, it is noteasy to make a general statement about thenutritive value of mushrooms. Species likePleurotus eous provide nutritive value compa-rable to that of meats and milk, while specieslike Pleurotus ostreatus due to low proteincontent and deficiency in some essential aminoacids have a low nutritive value (Zakia Banoand Rajarathnam, 1982). In view of the highcost and low efficiency of some forms of meatproduction, future diets are likely to emphasizethe vegetarian, thus giving mushrooms a spe-cial status as a useful food in the future. Recentanalyses proved that 200 g of mushrooms canreplace 100 g of meat (Souci et al., 1989).

Biological Value (BV) and Essential AminoAcid (EAA) Index of Pleurotus sajor-caju var-ied from 31 to 67 and 39 to 72, respectively.The limiting EAA were cysteine, isoleucine,phenylalanine, tryptophan, and valine (Bisariaet al., 1987). Six edible Thai mushroom spe-cies were also evaluated for their protein di-gestibility in vitro (Surinrut et al., 1987). BV ofAgaricus bisporus was 59.9% while that ofLactarius deliciosus 68.91% (Stankeviciene andUrbonas, 1988). Co-efficient of digestion ofChinese and Polish varieties of Lentinus edodesby pepsin and pancreatin was 77 and 60% re-spectively (Lasota and Sylwestrazak, 1989).Protein quality of several species of Pleurotuswas high and almost corresponding to that ofanimal derived protein (Eder and Wuensch,1991).

IV. BIODEGRADATIVE CAPACITIES

Most of the mushrooms species have beenrecognized for their property of degradation ofthe natural lignocellulosic wastes, in their origi-nal form or preformed (composted) form. Ingeneral, the plant residues like cereal strawscontain about 35% cellulose, 28% hemicellu-lose, and 25% lignin. These values vary with

the plant material, and maturity. The lignincontent is invariably high in the wood wastematerials. In simple terms, the fungi havingpreference to utilize cellulose and hemicellu-lose leave behind a brown residue of lignin andsuch species are called “Brown-rots” while theother group degrade strikingly the lignin com-ponent besides holo-cellulose, leaving behinda white residue (eventually cellulose) and suchfungi are termed the “White-rots”.

White-rots are the best lignin degraderswhich completely metabolize the complex poly-mer, and have been the most studied (Kirk andChang, 1981; Crawford and Crawford, 1984).Most of them, however, have the enzymaticcapacity to use cellulose, hemicellulose, andother components of lignocellulosic matter as asource of carbon and energy; hence, total bio-mass breakdown usually occurs and lignin re-moval is accompanied by removal of polysac-charides (Kirk and Moore, 1972). Conversionof lignocellulose into human food (fruitingbodies) and animal feed (solid residue withimproved digestibility) makes use of thesemushroom species as an attractive alternativeto the concept of delignification.

Brown-rot fungi, which occur predomi-nantly on soft-woods, have scarcely been stud-ied for biotechnological purposes (Agosin et al.,1989), despite their unique ability to removestructural polysaccharides in fully lignifiednative tissues without significant depletion ofthe lignin fraction (Kirk and Highley, 1973).This makes them potential candidates for thedirect bioconversion of softwood polysaccha-rides into fermentable sugars (Kirk, 1983).Furthermore, the residue remaining after de-cay — mainly lignin — has a potential as asource of other valuable products (Rajarathnamand Zakia Bano, 1989). Therefore, brown-rotfungi could provide a new saccharification sys-tem for lignocellulosic substrates, which mayallow the integral use of these abundant lowcost materials.

Cowling (1961) and Cowling and Brown(1969) suggested that the basic mechanismemployed by these fungi to degrade wood is

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related to their capacity to depolymerize cellu-lose during the initial stages of decay. It hasbeen proposed (Koenigs, 1974; Highley, 1977)that cellulose depolymerization opens up thewood cell wall, allowing cellulolytic andhemicellulolytic enzymes of the brown-rot fungito reach their substrates despite the presence oflignin. Among structural polysaccharides,hemicellulolytic and particularly glucomannans,are preferentially degraded during colonizationof soft-wood by brown-rot fungi (Kirk andHighley, 1973). However, the mechanism em-ployed by these fungi to remove the hemicellu-lose fraction and its role in the opening of thewood cell wall has received very little attention(Wolter et al., 1980; King and Fuller, 1968).

One of the strategies developed to utilizesignificant quantities of lignocellulosic wastes,generated annually due to photosynthesis, isthe culturing of edible mushrooms by solidstate fermentation (Chang and Miles, 1991). Itaims at producing nutritionally valued and validforms of biomass, with eventual scope for theeasiest means of separating the biomass fromthe growth substrate. Obviously, the process isa concept of value addition. Production of ed-ible mushrooms is an economically viable pro-cess, being practiced in most parts of the world(Chang and Hayes, 1978). Lentinus edodes,Volvariella volvacea, and Pleurotus sajor-cajuconstitute three important commercially cul-tured mushrooms that exhibit varying abilitiesto utilize different lignocellulosics as growthsubstrates (Buswell et al., 1996).

Agaricus bisporus, the conventionallygrown white button mushroom falls under thecategory of white-rots, so also the species ofPleurotus, which have a pronounced ligninolyticactivity, whereas species of Volvariella unableto degrade lignin are categorized under thebrown-rots (Chang and Hayes, 1978). A num-ber of criteria have been employed by the re-searchers all over the world, to evaluate thedegree of substrate degradation by these fungi.Differential utilization of the different substratecomponents by different mushroom speciesduring their growth and fructification are also

considered in these references. In general, lig-nin is broken down mostly during the vegeta-tive phase, whereas more of holocellulose isdegraded during the fructification. Its consump-tion is almost the same during the long-livedphase of spawn run and short lived phase offructification (Chang and Hayes, 1978;Rajarathnam et al., 1979a, 1987b).

A. Degradation of Cellulose,Hemicellulose and Lignin

The ability of Pleurotus sajor-caju to bio-degrade the weed Saccharum munja and valueof spent substrate that compares favorably withthe dry cow feed ration was studied (Gujaralet al., 1987). One of the four strains of Pleurotustested to degrade flax shive showed maximumactivities of laccase and polysaccharide degrad-ing enzymes, that could be correlated with highweight loss, reduction in the yield of lignin andholo-cellulose (also their degree of polymer-ization). Flavonoid type compounds detectedin the crude extract of flax shive might beresponsible for the increase in the productionof mushroom primordia (Sharma, 1987). Theco-culturing of Panus tigrinus and Poriavaillanti was more efficient in wheat strawlignocellulose degradation than mono-cultures (Ivanova, 1988). Co-culturing of strainsof Pleurotus sajor-caju, Phanerochaetechrysosporium and Trametes versicolor alsocaused increased degradation of native lignin,polymeric carbohydrates and IVDMED, overreduced lengths of incubation periods (Asiegbuet al., 1996a,b). A solid medium containing1.6% agar and 0.2% wood filings, with theinclusion of guaiacol was useful in isolation oflignin degrading mushroom species; strains ofCoriolus versicolor and Phanerochaetechrysosporium (Nishida et al., 1989) were foundto be active lignin degraders. Bioefficiency ofa combined submerged and solid substrate fer-mentation for the conversion of lignocelluloseof wheat straw was studied (Viesturs et al.,1987). A preliminary exploration on biological

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recycling of rice straw degraded by Pleurotussajor-caju for food, fuel and fertilizer is de-scribed (He et al., 1985). Thirty white-rot spe-cies were assessed for their ability to selec-tively degrade lignin (Otjen et al., 1987).

Samples from conventional compost takenat various stages of the growth of Agaricusbisporus were analyzed for changes in 80%ethanol and water extracts, monosaccharides inacid hydrolyzates of polysaccharides, ligninconcentration and structural features (Trudelet al., 1988). Similarly, changes in physico-chemical properties of wood by Coriolus ver-sicolor were observed (Bhandari and Bist,1989). Pholiota nameko during its growth andyield on sawdust-rice bran substrate in bottlesdecomposed lignin markedly during 20 to 50days of incubation, and cellulose was decom-posed during fruiting body formation. A 40%IVDMED was obtained with 100 days incuba-tion (Uzuki and Miyairi, 1991). Four strains ofspecies of Pleurotus, during their growth onsugarcane crop residues (for 30 days at 26°C)showed a strong ligninolytic activity, togetherwith variable cellulolytic and xylanolytic ac-tions. Pleurotus sajor-caju degraded 47% oflignin and 55% of cellulose; Pleurotus ostreatus,Pleurotus pulmonarius hybrid exhibited lowcellulolytic action (37%) and the highestligninolytic activity (67%) (Ortega et al., 1992).

Poria subacida, a white-rot fungus failedto degrade filter paper (cellulose) but degradedthe three lignin dimers, removing about 70% ofthe lignin, only 1.8% of the cellulose and 24.8%of the total weight of Japanese wood, i.e., thestrain was useful for removing lignin from woodwithout concomitant loss of cellulose (Enokiet al., 1988). Lentinus edodes could degradelignin and cellulose components of the soft-and hardwood sawdust to a similar extent (Dareet al., 1988). Phanerochaete chrysosporiumgrew faster and utilized the highest amount oflignin of both soft- and hard-wood pulp chips,compared with Pleurotus ostreatus and Lentinusedodes (Oriaran et al., 1989).

The differences in the patterns of release ofdegradatory enzymes by Pleurotus ostreatus

and Ceraceomyces sublaevis were correlatedwith the changes in thermogravimetric weightloss of the different components of flax shive(Sharma and Shekar, 1989). In a solid statefermentation of pine sawdust by the brown-rotfungus Gloeophyllum trabeum, oxygen wasfound critical for the wood decomposition; atwofold increase was observed when 21% O2

was employed as compared with 5% O2 (Agosinet al., 1989). The comparative degradation ofsugarcane chips (previously fermented by yeastemploying the EX-FERM process for sugarconversion to ethanol) by employing 12 white-rot species was evaluated (Table 3). Most fungishowed a preference for hemicellulose hydroly-sis over cellulose degradation. Sporotrichumpulverulentum and Dichomitus squalens showedgreater cellulolytic activity (Rolz et al., 1987).During a study of birch wood degradation,Coriolus hirsutus initially degraded lignin andhemicellulose and eventually also attacked cel-lulose; Pycnoporus sanguinea selectively de-stroyed lignin, with little damage to cellulose;Coriolus versicolor uniformly degraded allcomponents of the wood and formed abundantbiomass (Ozolina et al., 1987).

About 35% of cellulose and 39% of ligninof vine sprout wastes were degraded by Coriolusspecies and Phanerochaete chrysosporium in 10to 12 days (Kvesitadze et al., 1988). The regen-erated immobilized protoplasts of Hetero-basidium annosum showed higher lignin de-grading activity than free or immobilizedmycelia (Boettcher et al., 1988). Different ratesof wood-pulping and ligninolytic activity weredetermined for various white-rot species;Phellinus pini, Phlebia tremullosus, Poriamedullapans, and Scytinostroma galactinumwere selective for lignin degradation, unlikeCoriolus versicolor which caused a non-selective attack on all cell wall components(Blanchette et al., 1988). During a study of bio-logical pretreatments of coffee pulp with 26white-rot species, Stropharia pulverulentum andStropharia rugosoannulata significantly de-creased the lignin content and increased thewater soluble solids; Trametes versicolor was a

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TABLE 3Degradatory Changes in Sugarcane Bagasse by Mushroom Species

Ratio of degradationDry Soluble Lignin Cellulose Hemicellulose

weight solids loss loss loss Hemicellu- Hemicellu-loss (% dry lose lose

Species (g) weight) (% of control) IVDMED lignin cellulose

Phanerochaets 5.84 6.14 40.16 13.63 90.16 0.88 6.82 5.81chrysosporium

Agrocybe 0.00 7.79 31.29 0.00 20.76 0.42 2.01 Very highaegerita

Flammulina 0.00 3.50 37.46 4.41 16.13 3.73 1.30 3.19velutipes

Coprinus 2.07 3.93 37.89 2.82 24.83 8.53 1.99 7.74fimentarius

Ganoderma 1.14 1.93 40.58 1.37 20.02 8.62 1.50 12.67applanatum

Sporotrichum 8.13 6.62 47.75 24.39 41.83 10.07 2.67 1.51pulverulentum

Pycnoporus 3.52 6.15 32.33 5.12 31.27 10.78 2.91 5.30sanquineus

Dichomitus 2.90 4.39 35.94 14.06 24.39 12.44 2.06 1.52squalens

Isochnoderma 6.34 3.27 42.72 10.26 33.13 14.25 2.36 2.83resinosum

Pleurotus 5.35 0.34 40.70 12.55 27.14 15.54 2.03 1.90flabellatus

Bondarzewia 5.41 1.02 37.93 13.29 26.07 15.80 2.09 1.72berkeleyi

Coriolus 6.10 2.80 38.89 0.00 30.91 19.69 2.42 Very high

Adapted from Rolz et al., 1987

very fast grower and showed the highest ratesof holocellulose and lignin degradation; mostof the species preferred hemicellulose over cel-lulose (Rolz et al., 1988).

The degradation of wheat straw lignin byPleurotus sajor-caju increased under the influ-ence of CO2 (0 to 20%) in the atmosphere andthen started declining at higher levels. Themaximum loss of lignin (39.7%) was found incultures grown with passive air exchangethrough cotton plugs (Zadrazil and Puniya,1994). Pleurotus sajor-caju along withPseudomonas and urea, could render bettercomposting of coir pith (waste after processingof coconut fiber) involving significant reduc-tion in C:N (Thilagavathi et al., 1994). Corre-

lation between the biodegradability of strawcell-wall associated with polysaccharidases ofcultures of Scytalidium thermophilium,Pleurotus ostreatus and Lentinus edodes, andlignin or N contents of straw were significantlypositive. Correlations between biodegradabil-ity and ash contents were negative (Savoie et al.,1994). Inhibition of decay by Irpex lacteus wasobserved for test blocks treated with resin acids(abiotic and dihydroabiotic) — the major acidsof pine seed cones (Eberhardt et al., 1994).Proanthocyanidin polymers (condensed tannins)of conifer seed cones, in vitro, inhibited thegrowth of Ceratocyctis coerulesscens andSchizophyllum commune. It is apparent thatthese components contribute to the natural

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resistance of conifer seed cones to the fungaldegradation.

Degradation and water solubility of the lig-nin by white-rot species was increased depend-ing on the glucose concentration in the medium(Haars et al., 1986). Lower than 20% oxygenin the gaseous phase adversely affected the lossof organic matter, the lignin degradation andthe change in straw digestibility with Pleurotussajor-caju and Pleurotus eryngii (Kamra andZadrazil, 1986). Six of the eight white-rot fungiviz, Phanerochaete chrysosporium, Chryso-sporium prunosum, Phlebia radiata, Coriolusversicolor, Trametes cingulata, and Bjerkanderaadusta degraded lignin rapidly (mineralizationrate: 0.5 to 1% h–1) (Leisola et al., 1987). Par-tially reduced oxygen may play a role in theinitial degradation of cellulose and lignin inwood by cultures of brown-rot fungi; the 1-elec-tron oxidation activity was determined by mea-suring ethylene production from 2-Keto-4-thiomethyl-butyric acid. Ethylene productionwas related to the degradation of lignin, cellu-lose and wood itself (Enoki et al., 1989).

Loss of organic matter ranged from 10 to40% and that of lignin from 28 to 39% of wheatstraw in solid state fermentation by differentlignolytic species. Ganoderma lucidum,Pleurotus eryngii and Pleurotus sajor-cajudegraded hemicellulose preferentially over cel-lulose, while Polyporus caperatus andPolyporus sanguineus degraded cellulose inhigher proportions. Preferential degradation ofhemicellulose over cellulose appeared to berelated to the increase in digestibility in vitro offermented straw. Ganoderma lucidum recordedthe highest increase in digestibility (42%) withminimum loss of total dry matter (Singh andSrivastava, 1990). The ability of 45 species todegrade wheat straw and beech wood was stud-ied. Trametes versicolor produced an impor-tant degradation of lignin and increased sub-strate digestibility, but it caused high weightlosses and gave rise to similar decay patternson both substrates. A preferential degradationof lignin was produced during straw transfor-mation by Pleurotus eryngii. The increase of

soluble lignin and, decreases of lignin contentand H/C ratio defined the degradation tendency(Valmaseda et al., 1990). During fermentationof alkali treated corn stalks by Pleurotus sajor-caju, besides the degradation of holocellulose,the lignin was depolymerized into oligolignolsof progressively lower molecular weight(Chahal and Hachey, 1990). The alkaliphilicwhite-rot fungus, Coprinus fimetarius, degradedthe components of wheat straw under an opti-mized set of cultural conditions (pH-9.0, mois-ture = 65%; temperature = 37°C, for 21 days);45% of lignin, 42% cellulose and 72% hemi-cellulose were biodegraded (Tripathi andYadav, 1991).

Wheat straw fermentation by Strophariarugosoannulata was followed by pyrolysis gaschromatography (Chlavari et al., 1988). Pyroly-sis peaks and the energy release pattern of thelignocellulosic materials were correlated to thedegradation of compost and straw by Agaricusbisporus and Pleurotus ostreatus, respectively(Sharma ad Shekar, 1990). During the growthof Pleurotus and Agrocybe strains on wheatstraw and poplar prunings, the formation ofsoluble lignin fractions was followed by H1

NMR spectroscopy, which is proposed as asuitable method for preliminary investigationson the mushroom’s ability to degrade lignin(Pasetti et al., 1995). CP-MAS NMR and FT-IR spectroscopy have been employed as non-destructive methods to gain insight into themodifications at a molecular level, the cell wallcomponents undergo, during attack by thewhiter-brown-rot species. A solid state NMRtechnique was described to assess the level ofwood degradation by white-rot and brown-rotfungi (Gilardi et al., 1994). A quantitative ap-proach based on the integration of CP-MASNMR spectra showed that spruce lignin wasdegraded to 77% of its weight by brown-rotspecies and to 39% by white-rot species (Gilardiet al., 1995). During a study of wood decay byPhanerochaete chrysosporium, Trametes ver-sicolor and Dichomitus squalens, followed byC13 NMR, there appeared to be slight prefer-ence to the degradation of amorphous cellulose

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over crystalline cellulose and the syringyl toguaiacyl ratio of the lignin appeared to de-crease at higher weight losses (Davis et al.,1994a). While conducting a solid state C13

NMR study of the wood decay by the white-rots, Phanerochaete chrysosporium, Trametesversicolor and Dichomitus squalens both lig-nin and carbohydrate fractions of the woodwere removed almost evenly, showing no largepreference for either wood component; thereappeared to be a slight preference for amor-phous over crystalline cellulose (Davis et al.,1994b).

During a study of ultrastructural patternscharacterizing wheat straw degradation by theligninolytic fungi, Phanerochaete chryso-sporium and Trametes versicolor, the less lig-nified tissues were degraded first, whereas thexylematic and sclerenchymatic fibers under-went a delayed attack (Barrasa et al., 1995).Morphological changes in sawdust caused byCorriolus versicolor by TEM were followed;the soft-wood lignin was degraded more slowlythan the hard-wood lignin (Highly andMurmanis, 1987). Lignin distribution in cellwalls of birch wood decayed by several white-rot basidiomycetes was studied (Blanchetteet al., 1987). X-ray microanalysis was used totrace the wood decayed by the white-rot spe-cies Phellinus pini and Phanerochaetechrysosporium (Otjen et al., 1988). Hemicellu-lose within cells of birch wood degraded byCoriolus versicolor, Phellinus pini, andFomitopsis pinicola was determined using pe-riodic acid-thiocarbohydrazide-silver protein-ate coupled with energy-dispersive X-ray mi-croanalysis scanning electron microscopy(EDXR-STEM) (Blanchette et al., 1988). Pref-erential utilization of lignin and hemicellulosein wood, by Phanerochaete sanguiea was tracedby X-ray diffraction (Ioelovics et al., 1989).Ultrastructural and biochemical aspects of li-gnocellulose degradation by Coriolus versicolorwere studied (Fraser, 1989). TEM studies ofdifferentiation between cellulose and lignindegradation of wheat straw delignified byPleurotus ostreatus have indicated the tech-

nique as a possible valuable tool to monitorbiological delignification during industrial hy-drolysis of lignocelluloses (Schiesser et al.,1989). Using antibodies raised against manga-nese dependent peroxidase (Mn-P) (lignin-de-grading enzyme) and TEM immunocytochem-istry, the spatial distribution of Mn-P duringdegradation of wood and wood fragments byPhanerochaete chrysosporium and Lentinusedodes was studied (Andrawis and Kahn, 1990).

B. Mechanism of Lignin Degradation

Lignin is a more complicated non-carbohy-drate, heteropolymer of phenyl-propane unitsand its biodegradation is not simple. Prefer-ence of the fungal species to attack units andmodels of lignin, cultural conditions favoringlignin degradation, intra-molecular changes andspectral features during lignin degradation, thedegraded products as well as the possible routesof ultimate mineralization of lignin, are dis-cussed here.

White-rot fungi, Heterobasidium annosum,Pleurotus ostreatus and Stereum purpureumcaused the degradation of hardwood Kraft lig-nin, as shown by spectrophotometric studies at280 nm. Stereum purpureum had the highestlignin degrading activity (Stevanovic et al.,1988). Coriolus villosus may be more usefulfor studying ligninolytic systems than the usu-ally used Phanerochaete chrysosporium strains,since the former was able to unambiguouslymetabolize hydrolytic lignin and dioxane iso-lated lignin from spruce sawdust (Zolotarevet al., 1990). Lignin biodegradation was corre-lated apparently to the carbohydrates (espe-cially glucose) added to the medium whileculturing Pleurotus ostreatus (Kim et al., 1986).The influence of asparagine (up to 1.6%) addedas a N source favored lignin degradation ofwood by Pleurotus ostreatus, Pleurotuscornucopiae, Sporotrichum pulverulentum,Phanerochaete chrysosporium, Ganodermalucidum, Lentinus edodes, and Pholiota nameko.Anymore N added variedly influenced lignin

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degradation by the different species (Yamatotoet al., 1986).

Phanerochaete chrysosporium was dem-onstrated to degrade β-O-4 lignin model com-pounds (Kawai et al., 1987). Possible pathwaysof oxidative aromatic ring cleavage of ferulicacid (a phenolic model lignin compound) byLentinus edodes were presented (Ahn and Lee,1986a,b). The most active species in solubiliz-ing 14C β-lignins were Polyporus pinsitus andPolyporus platensis (up to 45%) (Trojanowskiet al., 1987). Degradation of a non-phenolicβ-O-4 lignin substructure model compound byCoriolus hirsutus resulted in the formation of10 metabolites, which were identified byGC-MS (Yoshihara et al., 1988). Model β-l-lignin compound was more actively decom-posed than β-O-4 type by Panus tigrinus andCoriolus versicolor (Golovleva et al., 1989).Several products of metabolism and aromaticring cleavage of 4-methoxy (Figure 2) and 3,4-dimethoxy cinnamic acids from ligninolyticcultures of Lentinus edodes were isolated andidentified (Figure 3) (Crestini and Sermanni,1994).

The degradation of wheat straw lignin byStropharia rugosoannulata can be monitoredthrough FT-IR spectroscopy (by comparison ofthe FT-IR spectra of the different straw prepa-rations) (Buta et al., 1989). Tyromyces lacteusand Coriolus hirsutus catalyzed lignin degra-dation in rye and flax straw; up to 40% ligninwas degraded by 15 days of incubation. UVand IR spectroscopy revealed that lignin degra-dation was associated with cleavage of methoxyland hydroxyl groups of the lignin molecule(Babits-Kaya et al., 1990). Mycelial pellets ofCoriolus versicolor (after a month starvation)oxidized the milled wood lignin and increasedthe amount of carbonyl and carboxylic acidgroups during incubation (Morohoshi andHaraguchi, 1987a,b). Urea supplementation ofthe growth medium enhanced the wood lignindegrading capacity of Coriolus hirsutus(Yoshihara et al., 1987). With increased degreeof wood decomposition by Coriolus hirsutus, ashift of molecular weight distribution of the

isolated milled wood lignin toward lower mo-lecular weights was observed along with anincrease in the UV absorption intensity at 280nm, apparently due to the increased formationof chromophoric structures. Nitrobenzene oxi-dation data showed syringyl structures (Ozolinaet al., 1988). A decrease in the syringyl/guaiacylratio observed with both Flammulina velutipesand Trametes versicolor, indicated the prefer-ential degradation of non-condensed (syringyltype) lignin units. An increase in the relativeabundance of aromatic carboxylic acids sug-gested that the oxidative transformation of lig-nin unit side-chains was occurring; this phe-nomenon was prominent with Flammulinavelutipes (Pal et al., 1995) (Table 4). The ligninsulfate decrease in wood flour in solid statefermentation by Coriolus versicolor was usedto measure lignin degradation; a mathematicalequation was proposed (Kakezawa, 1989).

The existence of a redox cycle leading tothe production of H2O2 in the white-rot fungusPleurotus eryngii was confirmed by incuba-tions of 10-day-old mycelium with veratryl (3,4-dimethoxybenzyl) and anisyl (4-methoxy-benzyl) compounds. Veratraldehyde andanisaldehyde were reduced by aryl-alcoholdehydrogenases to their corresponding alcohols,which were oxidized by aryl-alcohol oxidasesproducing H2O2. Possibly anisaldehyde is themetabolite produced by Pleurotus eryngii forthe maintenance of the redox cycle (Guillenand Evans, 1994). The mechanism of degrada-tion of phenolic β-1-lignin substructure modelcompounds (by laccase) of Coriolus versicolorwas studied. Based on the structure of degrada-tion products and 180 isotopic experiments, itwas established that three types of reactionsoccurred via phenoxy radicals of substrates(caused by laccase): (1) C-α-C-β cleavage (be-tween C1 and C2 atoms); (2) alkyl-aryl cleav-age (between C1 atom and the aryl group) and(3) C-α and (C1) oxidation (Kawai, Umezewaand Higuchi, 1988a).

Lignin intermediates by Phanerochaetechrysosporium and Coriolus versicolor wasfollowed by TLC and GC-MS (Umezawa and

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FIGURE 2. Pathways proposed for the metabolism of 4-metroxycinnamic acid. Metabolites detected in: (1) controlcultures, and (2) ferulic acid-induced cultures. (Adapted from Crestini and Sermanni, 1994.)

Higuchi, 1988). Me-esters of 4-O-acetylsyringic acid were postulated to have beenformed mainly by lignin degradation, during

the study of Quercus wood decay by Lentinusedodes. Using 14C Phenylalanine (during thedegradation of milled wood lignin by Lentinus

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FIGURE 3. Pathways proposed for the metabolism of 3,4 -dimethoxycinnamic acid. Metabolites detected in: (1)Control cultures, and (2) induced cultures. (Adapted from Crestini and Sermanni, 1994.)

edodes), it was shown that vanillic acid andveratryl alcohol were produced via two routes,i.e., the lignin biodegradation and de novo syn-thesis, and the former might be correct as themajor route (Kofujita et al., 1989). A first evi-dence indicating the possibility that the acetallinkage was one of the intermonomer linkages(in lignin) formed in the metabolism ofsyringaresinol structure of lignin by Coriolusversicolor was adduced (Katayama andFukuzumi, 1989). In a medium where phenoloxidase was actively produced by Coriolusversicolor, the first evidence of aromatic ringfission of biphenyl lignin structure was demon-strated (Katayama et al., 1989). Laccase puri-fied from Trametes versicolor oxidized 2,6-

dimethoxyphenol and syringaldazine in hydro-phobic solvents presaturated with H2O and inhydrophilic organic solvents, provided thatsufficient water was added (Milstein et al.,1989). The kinetics of straw SSF with Trametesversicolor and Pleurotus ostreatus was investi-gated to characterize the process of deligni-fication. High levels of H2O2 producing aryl-alcohol oxidase throughout the straw SSFoccurred only with Pleurotus ostreatus(Valmaseda et al., 1991). The brown-rot fungialso preferentially attacked syringyl structuralunits, but degraded all phenol precursors at amuch slower rate than the white-rots, and didnot produce excess vanillic acid (Hedges et al.,1988). Polymerization and depolymerization

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TABLE 4Chemical Changes in Bagasse Lignin Due to SSF by Trametesversicolor and Flammulina velutipes for 40 Days

FlammulinaControl Trametes versicolor velutipes

H:G:S 9:35:56 10:38:52 9:43:48S/G 1.6 1.4 1.1Acid/(aldehyde + ketone) 0.25 0.27 0.30Cinnamic acids/H:G:S 3.03 2.84 2.284-Hydroxybenzoic acid (µmol g–1) 0.82 1.57 3.53Vanillic acid (µmol g–1) 3.92 7.27 14.76Syringic acid (µmol g–1) 4.33 7.53 12.52

Note: H:G:S = p-hydroxyl phenyl:guaiacyl:syringyl.S:G = Syringyl:guaiacyl.

Adapted from Pal et al., 1995.

of lignin were noticed with the cultures ofCoriolus versicolor (Morohoshi et al., 1987a,b).Haraguchi (1986) has discussed the subject oflignin degradation by Coriolus versicolor andPhanerochaete chrysosporium.

Homoveratric acid degradation was ob-served in cultures of Pleurotus eryngii lackinglignin peroxidase (Li-p) activity, suggesting thatenzyme systems lacking Li-p could be respon-sible for natural degradation of lignin (Roveland Metche, 1986). Aromatic ring opening ofcinnamate structures lacking a free phenolicgroup was possible through incubation ofLentinus edodes extracellular enzymes fromferulic acid induced cultures (Giovannozziet al., 1986). Both Pleurotus eryngii andPhanerochaete chrysosporium caused a sig-nificant decrease in the relative amount of phe-nolic lignin units, during the degradation pro-cess, despite differences in the enzymicmachinery (Nigam et al., 1987). The pathwayof degradation of vanillyl and veratryl alcoholby Lentinus edodes extracellular enzymes wasfound different from other white-rot species;several products of side chain oxidation andaromatic ring cleavage were isolated, from in-cubations; however, veratraldehyde, as the ma-jor product, was not found as a final metabolite(Kinugawa et al., 1986). Requirement of only

partial delignification for maximum digestibil-ity was confirmed by degradation of wheatstraw with alcaliphic Coprinus species (Yadav,1988).

C. Degradatory Enzymes

Species of mushrooms have the biosyn-thetic potentialities to secrete and produce awide spectrum of enzymes, which have en-abled them to thrive over a range of plant wastes,to biodegrade the growth substrate(s), utilizethe degraded products, as their energy source,as well as building up of the biomass. Thus, theenzymes have two distinct phases in mush-room metabolism viz., for the function of de-grading the constituents for growth substrateand for the function of building up of the bio-mass-mycelium and fruiting bodies. In addi-tion, they secrete a third group of enzymes,mainly constructive, which tend to operate forthe respiratory metabolism, for physiologicalmaintenance of cells, production and dischargeof the basidiospores — the main and ultimatefunction of a mushroom to render perpetuationof the species. A gross consideration of theseaspects drawing examples from the availableliterature would emphatically pronounce the

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capabilities for mushroom species to generatethe enzymes for the functions of degradation,biomass construction and maintenance of thecell physiology. The latter two are dealt with inSection V.N.

The crude enzyme of Coriolus versicolorcaused changes in the chemical structure ofprotolignin, as a result of dearomatization(Nakamura et al., 1989). Lentinus edodes pro-duced a range of extracellular degradatory en-zymes such as cellulases, hemicellulases, fun-gal cell-wall-degrading enzymes, oxidativeenzymes, acid phosphatases, and acid protein-ases (Mishra and Leatham, 1990). Differencein degradability of protoligin by compatiblemonokaryons of Coriolus hirsutus comparedwith the dikaryon was elucidated (Yoshiharaet al., 1989). While monitoring the degradatoryenzymes at different depths throughout fruitingproduction, in a deep solid-substrate culture ofAgaricus bisporus, endocellulase activity de-clined steadily with increase in depth and wasalmost undetectable beyond a depth of 0.9 m inthe early stages of mushroom cropping. Laccaseactivity within the substrate close to the fruit-ing surface declined rapidly at the onset ofmushroom fructification but at a depth of 0.9m, laccase activity was 4-fold that found in theuppermost layer and the expected decline inactivity at the onset of fructification was de-layed. The implications of the enzymic patternwere related to the productivity of mushroomsfrom the substrate (Smith et al., 1989). Enzy-mic decomposition of bean and pea shells us-ing water extracts of pine/rice straw, colonizedand yielded by Pleurotus ostreatus was ob-served (Szebiotko et al., 1990).

At 24 h, a cellulase enzyme complex fromMorchella conica achieved 35.5% saccharifi-cation of microcrystalline cellulose (Avicel)with glucose 84.2% of the total reducing sugarsliberated; similar values for commercial cellu-lase were 31.2 and 52%, respectively (Manzoniand Cavazzoni, 1994). The cane top hemicellu-lose was excellently saccharified by a combi-nation of xylanases, produced extracellularlyby a mycelial strain of Termitomyces clypeteus

(Khowala et al., 1989). Lyophyllum ulmarium(grown on sawdust medium) was the biggestproducer of cellulolytic enzymes among thecultivated basidiomycetes; the cellulase(s)(β-1,4-glucanase, β-glucosidase) and xylanaseactivities in sawdust medium greatly increasedcorresponding to increasing protease activities,just after the formation of fruiting primordia(Amano et al., 1992).

Varying abilities of three species viz.,Lentinus, Volvariella, and Pleurotus to utilizedifferent lingoncellulosic substrates are reflectedby qualitative variations in the major enzymicdeterminants (i.e., cellulase and ligninase) re-quired for substrate bioconversion. For example,Lentinus edodes, which is cultivated on highlylignified substrates such as wood or sawdust,produces two extracellular enzymes, namely,viz. (which have been associated with lignindepolymerization in other fungi) manganeseperoxidase and laccase. Conversely, Volvariellavolvacea, which prefers high cellulose, low lig-nin-containing substrates produces a family ofcellulolytic enzymes including at least fiveendoglucanases, five cellobiohydrolases andtwo β-glucosidases, but none of the recognizedlignin-degrading enzymes (Buswell et al.,1996).

Phenol oxidase activity in oak sawdust in-creased with the cold shock used to inducefruiting in Lentinus edodes (Okeke et al., 1994).The mushroom phenol oxidase(s) could possi-bly serve as agents to transform phenolics insoil (Claus and Filip, 1987). Lignin-degradingenzyme that converts syringyl-glycerol-β-syringyl ether to 2,6-dimethoxyphenol and thatdegrades lignin to lower molecular weight sub-stances was produced by cultivation of Coriolusin a synthetic medium (Koide et al., 1987). It ispresumed that the lignin model glucosides wereformed enzymically by the transglucosylationof intracellular glucosidase induced into cello-biose cultures (but not in glucose media cul-tures) with Coriolus versicolor or Tyromycespalustris (Kondo and Imamura, 1988).

Immunogold staining revealed a higherconcentration of ligninase near and on the

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plasma membrane, but not on the hyphal wallof extracellular membraneous structures, ofwood-degrading mushroom species (Messneret al., 1987). Transmission electron microscopyof immunogold labeled sections was used toshow the localization of lignin peroxidase andlaccase, in ultrathin sections of hyphae ofCoriolus versicolor. Both the enzymes werelocalized in the fungal cell walls and mucilagelayers of both generative and skeletal hyphae,whereas lignin peroxidase but not laccase wasalso evident adjacent to the plasma membrane(Gallagher et al., 1989).

D. Ligninolytic Enzymes

Lignin as a 3-dimensional polymer is foundabundantly in wood and plant tissues (Sarkanenand Ludwig, 1971). Apparently, lignin is thesecond most abundant phytogenic organic sub-stance in the biosphere, surpassed only by cel-lulose. It is composed of phenyl propanoid unitsinterconnected by stable C-C and C-O bonds.The heterogeneity and complexity of its struc-ture confers resistance to microbial attack. Thewhite-rot species are unusual among microor-ganisms in that they are able to mineralize allcomponents of native lignin into carbon diox-ide and water (Eriksson et al., 1990). White-rotspecies like Phanerochaete chrysosporiumproduced numerous extracellular ligninperoxidase(s) and/or manganese peroxidase(s)that were able to initiate the depolymerizationand degradation of lignin and, its oligomersand monomers (Hammel et al., 1993; Wariishiet al., 1991). Phenol oxidases such as laccase,present in many white-rot species but not inPhanerochaete chrysosporium, are also thoughtto participate in the oxidative degradation oflignin (Reinhammar, 1984; Morohoshi, 1991;Thurston, 1994). Ligninases use H2O2 as theterminal acceptor of electrons removed fromlignin or other substrate, while laccases useoxygen.

Lignin biodegradation by white-rot fungi isan oxidative process in which H2O2 plays an

important role (Crawford and Crawford, 1984).The lignin-degrading system and enzymes in-volved have been studied quite extensively inPhanerochaete chrysosporium. When activelydegrading lignin, this strain produces extracel-lular H2O2 (Faison and Kirk, 1985) and a num-ber of peroxidases that were able to oxidizeseveral lignin model compounds (Tien and Kirk,1983; Glenn et al., 1983; Huynh and Crawford,1985). One of the peroxidases designated, lig-nin peroxidase (Li-p) (Tien and Kirk, 1983)was found to be induced by veratryl alcohol,which is synthesized de novo by the fungusduring its ligninolytic phase (Fauson et al.,1986). The enzyme is distinctly assayed by theoxidation of veratryl alcohol to veratraldehydein the presence of H2O2. In the same fungus,many enzymes have been proposed for H2O2

generation, including intracellular enzymes suchas glucose oxidase and glucose-2-oxidase(Eriksson et al., 1986), and more recently anextracellular oxidase (Kersten et al., 1987).H2O2 producing oxidases have also been re-ported from other ligin degrading fungi, in-cluding an extracellular aromatic phenol-oxi-dase from Polystictus versicolor (Farmer et al.,1960). The enzymes involved in lignin degra-dation appeared quite different, even thoughthis white-rot fungus has been recognized as alignin degrader (Trojanowski and Leonowicz,1986; Leatham, 1986; Leatham et al., 1991).

1. Lignin Peroxidases

Ligninase (lignin peroxidase) from Phaner-ochaete chrysosporium has been purified andits mode of action studied in several laborato-ries (Buswell and Odier, 1987; Kirk and Farrell,1987). In the presence of H2O2, the extracellu-lar hemeprotein peroxidase catalyzes the one-electron oxidation of aromatic nuclei generat-ing cation radicals (Kersten et al., 1985;Hammel et al., 1985; Hammel et al., 1986a).Subsequent spontaneous reactions of these cat-ion radicals lead to extensive degradation oflignin model compounds (Buswell and Odier,

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1987; Kirk and Farrell, 1987; Higuchi, 1986).A major reaction is cleavage between Cα andCβ in the propyl side chains.

Cα-Cβ cleavage per se should result in de-polymerization of lignin. However, studies withmodel dimers representing the major ligninsubstructure — the aryl glycerol-β-aryl etheror β-O-4 type — have shown that Cα-Cβ cleav-age by ligninase liberates a phenolic productfrom the ether-linked aryl moiety (Higuchi,1986; Tien and Kirk, 1984). Ligninase wasshown to dimerize 4-t-butylguaiacol (Tien andKirk, 1984), indicating that it acts as a phenol-oxidizing enzyme such as laccase or horserad-ish peroxidase. Thus, the phenolic degradationproducts, and the phenolic units already presentin lignin (Adler, 1977) would be expected to bepolymerized by ligninase. In fact, some inves-tigations have shown that ligninase actuallypolymerizes lignin (Haemmerli et al., 1986a;Kern and Kirk, 1987).

Intact ligninolytic cultures of Phaner-ochaete chrysosporium, however caused a rapidand extensive depolymerization of lignin (Chuaet al., 1983; Leisola et al., 1983; Fenn and Kirk,1984; Faix et al., 1985), suggesting the exist-ence of a biochemical mechanism for prevent-ing phenol polymerization. Enzymatic reduc-tion of the oxidized phenolic products is onepossibility and a candidate enzyme is cello-biose: quinone oxidoreductase (CBQ-ase), anextracellular flavoprotein that was discoveredby Westermark and Eriksson (1974a,b), andBurdsall and Eslyn (1974). CBQ-ase catalyzesthe rather specific oxidation of cellobiose, form-ing cellobiono-5-lactone, with the transfer oftwo electrons non-specifically to quinones.CBQ-ase has been purified and characterized(Westermark and Eriksson, 1975, Ayers andEriksson, 1982; Kelleher, 1981). Westermarkand Eriksson (1974b) suggested that CBQ-asereduces phenoxy radicals as well as quinones.They demonstrated quinone but not phenoxyradical reduction. Although lignin degradationoccurs in the absence of CBQ-ase (Ander andEriksson, 1975), other enzymes with similarreducing activity (Green, 1977; Ishihara and

Nishida, 1983; Szklarz and Leonowicz, 1986)could have the same function in the absence ofCBQ-ase.

2. Manganese Peroxidases

A class of proteins structurally related tolignin peroxidases was subsequently identifiedin Phanerochaete chrysosporium (Glenn andGold, 1985; Paszczynski et al., 1985) andTrametes (Syn. Coriolus) versicolor (Johanssonand Nyman, 1987). These manganese depen-dent peroxidases function by oxidizing Mn2+ toMn3+ (Glenn and Gold, 1985; Glenn et al.,1986). Mn-peroxidases (Mn-p) are capable ofproducing H2O2 from reductants such as glu-tathione (GSH) using O2 as oxidant (Huynhet al., 1986b). The redox potential for Mn3+

(Eo = 1.54 V) is theoretically strong enough tocatalyze ligninase-like reactions under physi-ological conditions. An enzymatically gener-ated oxidized manganese species acting as anactive, diffusible agent in lignin biodegrada-tion is an attractive concept (Paszczynski et al.,1985; Huynh et al., 1986a,b; Glenn et al.,1987) — especially because of the size advan-tage of manganese over enzymes in penetratinglignocellulosic complexes. The ligninolyticactivity of the lignin degrading Lentinus edodeswas shown to be dependent on manganese ad-dition (Leatham, 1986). However, this ediblecommercial mushroom apparently lacks a lig-nin peroxidase capable of oxidizing veratrylalcohol in the absence of manganese. Forresteret al. (1990) demonstrated that Mn-p in Lentinusedodes in the presence of Mn3+ could also cata-lyze the oxidation of veratryl alcohol; the reac-tion was greatly stimulated by GSH. It is alsosuggested that chelated Mn3+ and lignin peroxi-dases may act in concert achieving a synergis-tic lignin degradation. To be consistent withexisting terminologies, the authors refer to theLentinus edodes-type enzyme as a “Mn-depen-dent lignin peroxidase”.

Mn-p activity was detected in the superna-tant liquid of the cultures of Phanerochaete

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sordida. Li-p and laccase activity were notdetected under a variety of different cultureconditions. The highest Mn-p activity levelswere obtained in nitrogen-limited culturesgrown under an oxygen atmosphere. The en-zyme was induced by Mn (Ruttimann-Johnsonet al., 1994). Three Mn-p isozymes were iden-tified and purified to homogenity; they wereactive in the same range of pH values (3.0 to6.0) and had optimum activities between 4.5and 5.0 pH. The three Mn-p isozymes isolatedfrom Phanerochaete sordida were glycosylatedhemeproteins with molecular masses of around45 kDa. The existence of a number of differentMn-p as well as Li-p isozymes was describedfor other white-rot species (Farrell et al., 1989;Jonsson et al., 1987; Maltseva et al., 1991). Theinvolvement of Mn-p (as a lignin-degradingenzyme) in the oxidative degradation of sev-eral important pollutants like pentachloro-phe-nol and other toxic chlorinated compounds(Hammel and Tardone, 1988; Lamar, 1992;Sarkar et al., 1988; Stott et al., 1983; Tatsumiet al., 1992; Valli and Gold, 1991) is well docu-mented.

3. Laccases

Laccase is a blue copper oxidase that cata-lyzes the 4-electron reduction of O2 to H2O dur-ing its oxidation of phenolics, aromatic amines,ascorbate and metal cyanides (Malmstrom et al.,1975). Although some substrates are potentialtwo electron donors, the blue oxidases are re-duced in one-electron step. This is due to thereduction mechanism in which Type-1 copperis the primary electron acceptor. The substrateradicals thus formed take part in further nonen-zymatic reactions. The laccase from Trametesversicolor had Type-1 and Type-3 coppersites of particularly high redox potential in com-parison with other blue copper proteins(Reinhammar, 1972, 1984). Futhermore, evi-dence was presented that laccase, like ligninperoxidase, plays a role in lignin degradation(Kawai et al., 1988a). Of the 12 methoxy ben-

zene congeners, laccase oxidized only 1,2,4,5-tetramethoxy benzene (Kersten et al., 1990).Apparently this is the first report of oxidationby laccase of aromatic nuclei bearing no hy-droxy or amino group, although it is well knownthat lignin peroxidase oxidizes such substrates(Buswell and Odier, 1987; Hammel et al.,1986b; Higuchi, 1986; Kirk and Farrell, 1987;Tien, 1987). Laccases have 10-fold higher Kcatvalues than Li-p with 1,2,4,5-tetramethoxy-benzene; the Kcat/Km values indicate that Li-p is only a slightly more efficient catalyst thanlaccase. Although extracellular laccase appar-ently has a role in lignin degradation in vivo(Ander and Eriksson, 1976; Kirk and Farrell,1987), several other reports have demonstratedthat in vitro, laccase preferentially polymerizeslignin-related substances rather than depoly-merising them (Huttermann et al., 1980;Leonowicz et al., 1985). Probably oxidation ofphenolics by laccase in vitro generates quinon-oid intermediates resulting in the initial forma-tion of dimers and subsequent spontaneouspolymerization of these dimers (Lundquist andKristersson, 1985). However, repolymerizationof lignin-derived phenoxy radicals might bediminished in some organic solvents in com-parison to aqueous solutions (Kazandijian andKlibanov, 1985). Immobilized laccase in or-ganic solvents showed good stability and hightolerance to elevated temperatures (Milsteinet al., 1989). The possible application oflaccases in the detoxification of various aquaticand terrestrial pollutants and in the treatment ofindustrial waste waters is advocated (Bollag,1983; Shuttleworth and Bollag, 1986). Laccasehas the advantage that it does not require theaddition of H2O2-like peroxidase, and it has abroader substrate specificity than tyrosinase.

4. Aryl-Alcohol Oxidases

Two veratryl alcohol oxidase (VAO) en-zymes were found in the cultured medium ofPleurotus sajor-caju that mineralizes ring-14C-labeled lignin (dehydrogenative polymer) when

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grown in mycological broth. Both the enzymesare glycoproteins and contain flavin prostheticgroups, with pH optima around 5.0. 4-Meth-oxybenzyl alcohol was oxidized most rapidly,followed by veratryl alcohol. Not all aromaticalcohols were oxidized, neither were non-aro-matic alcohols. Cinnamyl alcohol was oxidizedat the gamma-position. The VAO enzymes aptlyrepresent a significantly different route forveratryl alcohol oxidation from that catalyzedby Li-ps from Phanerochaete chrysosporium.The role of the oxidases in biodegradation mightbe to produce H2O2 during oxidation of ligninfragments. If VAO plays a role in lignin bio-degradation, it could be either through two elec-tron redox cycling or veratryl alcohol or ligninfragments, with H2O2 production from O2 or incombination with laccase, as a dehydrogenaseof aromatic compounds (Bourbonnais and Paice,1988). Sannia et al. (1991) have purified andcharacterized a VAO from the cultures ofPleurotus ostreatus. This enzyme oxidizedveratryl alcohol to veratraldehyde with a con-comitant reduction of O2 to H2O2. Its produc-tion did not seem to be induced by the presenceof veratryl alcohol, olive oil, sawdust, induline-At or Tween80 in the culture broth. Cinnamylalcohol was the most rapidly oxidized, whereasthe oxidation of coniferyl alcohol was lower.The possible role of a laccase and FAD-depen-dent aryl alcohol oxidase excreted by Pleurotusostreatus was investigated by Marzullo et al.(1995). They found that the VAO was able toreduce synthetic quinones, laccase-generatedquinonoids, and phenoxy radicals with con-comitant oxidation of veratryl alcohol toveratraldehyde. This cooperative action oflaccase and VAO also prevented the polymer-ization of phenolic compounds and reduced themolecular weight of soluble lignosulphonatesto a significant extent The production of anextracellular aryl-alcohol oxidase from thewhite-rot fungus Bjerkandera adusta was stud-ied under limitations of carbon and nitrogen.The purified enzyme consisted of two oxidases.Of the tested aryl-alcohols, the highest oxida-tion rate was obtained with anis alcohol. The

aryl-alcohol oxidase contained FAD as a pros-thetic group (Muheim et al., 1990a).

Of the three extracellular enzymes that havebeen implicated in lignin degradation bywhite-rot fungi (Li-p, Mn-p and laccase), onlyMn-p activity was detected in cultures ofPhanerochaete sordida grown under a varietyof different conditions. White-rot species havebeen shown to produce different combinationsof these three extracellular enzymes (Table 5).Phanerochaete chrysosporium, the most ex-tensively studied white-rot fungus producedseveral isozymes of Li-p and Mn-p, but nolaccase. In Phanerochaete sordida cultures, noLi-p or laccase could be detected, even underconditions in which secretion of these enzymesby other fungi was optimized. However, it wasnot possible to rule out the production of Li-p.Genes like those that encode Li-p were foundin this organism by using Southern blot tech-niques and therefore it is possible that the en-zymes could be induced in other culture condi-tions, for example, when growing on wood orsoil. Li-p activity was not detected in the com-post extracts, during the growth of Agaricusbisporus. A correlation between the activitiesof Mn-p and laccase and the degradation oflignin by Agaricus bisporus suggests signifi-cant roles of these two enzymes in lignin deg-radation by this mushroom.

Thus, the white-rot fungi are known toemploy a variety of extracellular oxidative en-zymes to cleave lignin. The best characterizedof these are the lignin peroxidases (Li-ps)(Edwards et al., 1993; Gold et al., 1989; Kirkand Farrell, 1987; Piontek et al., 1993; Pouloset al., 1993), which cleave polymeric ligninbetween C and C of its propyl side chain togive oxidized lignin oligomers (Hammel et al.,1993; Hammel and Moen, 1991). Otherligninolytic mechanisms exist however, per-haps allowing certain Li-p-negative fungi todegrade lignin (Perle and Gold, 1991;Ruttimann-Johnson et al., 1993; Wariishi et al.,1991), Li-ps are common to many white-rotspecies, and the evidence is strong that theyplay a role in ligninolysis (Hammel et al., 1993).

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TABLE 5Distribution of Extracellular Enzymes, Implicated in Lignin Degradation, in the White-Rot Species

Lignin ManganeseSpecies Laccase peroxidase peroxidase Ref.

Agaricus bisporus + – + Bonnen et al. (1994)Phanerochaete chrysosporium – + + Ruttimann- Johnson (1994)Phanerochaete sordida – – + Ruttimann — Johnson (1994)Dichomitus squalens + – + Perie and Gold (1991)Cereporiopsis subvermispora + – + Ruttimann et al. (1992)Phlebia brevispora + – + Ruttimann et al. (1992)Rigidoporus lignosus + – + Galliano et al. (1991)Panus tigrinus + – + Maltseva et al. (1991)Lentinus edodes + – + Forrester et al. (1990)Ganoderma colossum + – + Horvath et al. (1993)Phlebia radiata + + + Kantelinen et al. (1989)

Niku-Paavola et al. (1988)Coriolus versicolor + + + Jonsson et al. (1987)Phlebia ochraceofulva + + – Vares et al. (1993)Junghunia separabilima + + – Vares et al. (1993)

In Li-p-producing fungi, lignin degradationcoincides with Li-p secretion, and in most casesboth processes are functions of secondary(idiophasic) metabolism (Gold et al., 1989; Kirkand Farerell, 1987).

White-rot species which produce Li-ps gen-erally secrete a secondary metabolite, veratrylalcohol (VA) (Harper et al., 1990; Lundquistand Kirk, 1978), which is a substrate for Li-p(Tien et al., 1986). VA protects Li-p againstH2O2-mediated inactivation and has been pro-posed to act in vivo as a stabilizer for the en-zyme (Wariishi and Gold, 1989). This stabiliz-ing effect is probably responsible for theobservation that exogeneous addition of VAenhances Li-p secretion in certain white-rotspecies (Fauson et al., 1986). VA also promotesthe Li-p catalyzed oxidation of other moleculesthat are either inaccessible to the enzyme orrecalcitrant, by themselves, to enzymatic at-tack (Akamatsu et al., 1990; Haemmerli et al.,1986a,b; Hammel and Moen, 1991; Harveyet al., 1986; Paszczynski and Crawford,1991a,b; Wariishi et al., 1991). Some research-ers have proposed that VA participates in thesereactions by acting as a redox shuttle betweenLi-p and substrate (Akamatsu et al., 1990;Harvey et al., 1986; Popp et al., 1990). Others

have presented evidence that only one of theredox states in the Li-p catalytic cycle is ca-pable of oxidizing certain substrates and thatVA is required in these cases as a co-substratethat allows the enzyme to complete its turnover(Paszczynski and Crawford, 1991a,b; Tien et al.,1986). VA thus plays diverse roles in white-rotfungal metabolism. Jensen et al. (1994) havedemonstrated the biosynthetic pathway for VAin Phanerochaete chrysosporium as follows:Phenyl → alanine → Cinnamate → Benzoateand/or Benzaldehyde → VA. Its formation co-incides with the onset of ligninolytic activity(Kirk and Farrel, 1987; Lundquist and Kirk,1978).

Thus, the subject of lignin biodegradationis a field where much research is done, but it isstill open for more research. A proposed schemefor degradation of lignin, implicating the in-volvement of the various classes of oxidizingenzymes is depicted (Figure 4) (Leisola andGarcia, 1989).

E. Biological Pulping

A brief overview of the status of researchaimed at applying biotechnology in pulp and

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FIG

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9.)

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paper manufacture and a synopsis of the statusof relevant fundamental research are providedby Kirk and Eriksson (1990). Research onbiopulping, based on the ability of white-rotwood decay fungi to colonize wood rapidlyand degrade lignin, was pioneered at the Swed-ish pulp and paper Research Institute (STFI),where cellulaseless mutants of white-rot fungiwere developed and used in the partialdelignification of various lignocellulosematerials (Eriksson, 1988). A biopulping con-sortium in Madison, Wisconsin, has beencomprehensively investigating the concept ofbiopulping (Kirk and Chang, 1990; Myers et al.,1988). The consortium includes 17 pulp andrelated companies, the USDA Forest Service,Forest Products Laboratory, and the Universityof Wisconsin and is in cooperation with theUniversity of Minnesota. Lignin removal usingselective white-rot fungi in bioreactors withaspen, spruce, and pine chips ranged from 3 to37% in 4-week fungal pretreatments. Refinermechanical pulps prepared from the fungus-pretreated chips and from untreated controlchips were evaluated. Energy requirements fromrefining decreased by as much as 50% withfungus-pretreated chips. Burst, tear, and tensilestrength of hand sheets from the biopulped aspenmaterials increased, with the burst index in-creasing a maximum of approximately three-fold over controls. Brightness and light scatter-ing decreased, but bleachability was notadversely affected and properties of the handsheets overall were comparable to those ofchemically treated mechanical pulps.

Biopulping of sugarcane bagasse was stud-ied in a cooperative venture between the STFIand a Cuban laboratory. An energy saving ofabout 40% was achieved in a process using acellulase-less mutant of a lignin-degrading fun-gus followed by cold soda/thermo-mechanicalpulping (Johnsrud, 1987). There was improve-ment in pulp properties following treatmentswith various mushroom cellulases and xylanases(Noe et al., 1986, Jurasek and Paice, 1988;Senior, 1988; Feuntes and Robert, 1988;Uchimoto, 1988).

Whole living fungi were shown to be effec-tive in bleaching pine Kraft pulp in the labora-tory (Kirk and Yang, 1979). Promising resultswere obtained in Canadian laboratory studieswith hardwood Kraft pulp (Paice, 1989a,b).Use of enzymes from Lentinus lepideus,Pleurotus ostreatus, Tyromyces palustris,Coriolus versicolor, Ganoderma, and Pycno-porus coccinueus prevented the impairment ofpaper strength or sizing during its manufacture(Ueno et al., 1990). There was a desired bio-logical softening of cotton plant stalks(Balasubramanya et al., 1989) and other ligno-cellulosic wastes (Yamaguchi et al., 1995) bymushroom species for preparing pulp.

F. Kraft Pulp Discoloration

Residual lignin in Kraft pulp is highlymodified by the alkaline condensation reactionduring pulping and gives the pulp a character-istic dark brown color. This residual lignin iscommercially removed by bleaching with chlo-rine-based chemicals. It has been reported thatchlorinate products derived from lignin duringthese bleaching procedures are mutagenic(Ander et al., 1977; Rappe et al., 1989). Theyalso cause a waste treatment problem becauseof their toxicity and dark color. Therefore, en-vironmental concerns led to a search of alterna-tive ways to eliminate, or at least reduce, theuse of chlorine-based chemicals in bleaching.Because Phanerochaete chrysosporium andTrametes versicolor were studied intensivelyfor lignin degradation (Crawford, 1981;Eriksson and Lindholm, 1971, Higuchi, 1985;Kirk, 1971; Perez and Jeffries, 1992), muchresearch was carried out in an attempt todelignify and brighten unbleached Kraft pulp(UKP) by these fungi. Kirk and Yang (1979)were the first to recognize that Phanerochaetechrysosporium could partially delignify soft-wood UKP. It was also reported that hardwoodUKP treated with Trametes versicolor showedan increase in brightness and a correspondingdecrease in residual lignin concentration

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(Kirkpatrick et al., 1989; Paice et al., 1989a).Nishida et al. (1988) showed that the white-rotfungus IZU-154, which degraded wood ligninmore extensively and selectively than Phaner-ochaete chrysosporium and Trametes versi-color, delignified hardwood and softwood UKPand increased pulp brightness significantly. Inaddition, the use of chlorine-based chemicalsand the pollution load of waste liquor in bleach-ing of UKP were significantly reduced by thebiobleaching process, which combined an IZU-154 treatment and chemical bleaching (Fujitaet al., 1991; Fujita et al., 1993; Murata et al.,1992).

The white-rot fungus Polyporus (Trametes)versicolor was able to bleach and brightenunbleached hard-wood Kraft pulp within a fewdays, but soft-wood kraft pulps required longertreatments (Reid and Paice, 1994a). The effectof quinone-reducing and phenol-methylatingenzymes of Phlebia radiata and Phanerochaetechrysosporium on the yellowing (brightnessreversion) of mechanical pulp was studied;however, these treatments did not preventbrightness reversion, which indicated that re-actions other than methylation were respon-sible for the prevention of yellowing (Hatakkaet al., 1994).

White-rot fungi and their enzymes had adefinite effect in biological bleaching of Kraftpulp (Reid and Paice, 1994b). Enhancement ofbleaching of direct blue-1 with Myrotheciumverrucaria bilirubin oxidase or Trametes villosalaccase in the presence of various compoundswas demonstrated (Schneider and Pedersen,1995). Phanerochaete sordida was able tobrighten the pulp 21.4 points to 54% brightnessafter a 5-day in vitro treatment. A positivecorrelation between the level of manganeseperoxidase and brightening of the pulp wasobserved (Kondo et al., 1994). The white-rotfungus removed only 18.6% lignin from ricestraw in 3 weeks, but effected 99% decoloriza-tion of congo red dye in 9 days (Dey et al.,1994).

Hardwood Kraft pulp was bleached directlyby Coriolus versicolor to brightness as high as

67%; best bleaching was obtained when theinoculum was in exponential growth phase (Hoet al., 1990). Kraft hardwood pulps werebleached by treatment with mycelium ofCoriolus versicolor; the pulp showed an in-crease of 15% brightness and 1% decrease inlignin content compared with that of the un-treated Kraft pulp (Paice et al., 1989a,b). Useof polydimethylsiloxane (as oxygen carriers)in the cultures of Trametes versicolor aidedincreased fungal growth rate and oxygen up-take rate, which aided to increase pulp bright-ening (Ziomek et al., 1991). However, thedelignification rate in the biobleaching processis somewhat lower than that in the chemicalbleaching process. Attempts were made to de-termine the enzymologic basis of fungal bleach-ing using Phanerochaete chrysosporium andTrametes versicolor that produced laccase, lig-nin peroxidase (Li-p), and manganese peroxi-dase (Mn-p) (Dodson et al., 1987; Gold et al.,1984; Johansson and Nyman, 1987; Kondoet al., 1994; Reinhammar, 1984; Tien and Kirk,1983) — the enzymes involved in the oxidativebreakdown of lignin. Perez and Jeffries (1990)showed that increased synthetic lignin mineral-ization correlated with increase Li-p activity,not with increased Mn-p or laccase activity,and Li-p was reported to bleach UKP (Arbeloaet al., 1992; Farrell, 1987), and to facilitatesubsequent chemical bleaching (Olsen et al.,1989). However, there are some reports in whichthe role of Li-p in lignin biodegradation is ques-tioned. Paice et al. (1993) reported that Li-pactivity is not detected during biobleaching ofUKP by Trametes versicolor, and there areseveral lignin-degrading fungi that secrete Mnpand laccase but not Li-p (Galliano et al., 1991;Leatham, 1986; Nerud et al., 1991; Perie andGold, 1991). Mnp was found to depolymerizesynthetic lignin (Wariishi et al., 1991) and wasshown to be present at substantial levels duringbiobleaching with Trametes versicolor (Paiceet al., 1993). Mnp was produced by bleachingcultures of Trametes versicolor and the peakproduction of the enzyme occurred at the sametime as the maximum rate of fungal bleaching.

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Kondo et al. (1994) showed that cell-free, mem-brane-filtered components in the in vitrobiobleaching system were capable of deligni-fying UKP and that a positive correlation be-tween the level of Mn-p and brightening of thepulp was observed. By a new approach in whichthe enzyme assay was carried out with fungus-treated pulp, instead of with the extracted en-zyme from the fungus-treated pulp, cumulativeenzyme activity was determined. Mn-p wasshown to be the most important enzyme inbiobleaching of UKP by Phanerochaetechrysosporium and Trametes versicolor(Katagiri et al., 1995).

A cultivation system was developed, inwhich a membrane filter was used that pre-vented direct contact between hyphae and Kraftpulp, but allowed extracellular enzymes to at-tack the Kraft pulp. Table 6 depicts the resultsof in vitro bleaching by extracellular enzymesin the membrane system (Kondo et al., 1994).The well-known white-rot fungus Tyromycespalustris was inoculated as a control organism.

G. Decolorization of Waste Waters

Waste olive waters from the solid-liquidprocessing system were degraded in the liquid

cultures of white-rot fungus, Lentinus edodes.About 45% of biodecoloration and 75% of to-tal organic carbon reduction were achieved inless than 4 days. Over the same period, the totalphenolic content was reduced by 66%. A highlysignificant correlation was observed betweenthe decoloration, total organic carbon and totalphenols (Vinciguerra et al., 1995). Waste wa-ters from a small pulp mill were decolorizedwith Trametes versicolor. The fungus was usedin the form of pellets, allowing its use in largeamounts and eliminating the problem of recy-cling the biomass. The optimum pH and tem-perature for decolorization were 4.5 to 5.0 and25 to 35°C, respectively. With an effluent of18,500 color units, the maximum color reduc-tion of 92% with a COD reduction of 59% wasobtained (Mehna et al., 1995). Bajpai and Bajpai(1994) compared the ability of different organ-isms to decolorize pulp and pulp waste water.Phanerochaete chrysosporium and Coriolusversicolor were observed to be suitable for theefficient degradation of these effluents, but re-quirements for high oxygen tension and agrowth substrate constrained the practical ap-plication of fungal decolorization.

Laccase for use in the degradation of phe-nolics in water purification was manufactured

TABLE 6In Vitro Bleaching of Kraft Pulp with Mushroom Species

Delignification Brightness b

Species Membrane a (%) (%)

Tyromyces palustrisc P-filter 1.0 34.5C-filter 0.8 33.8

Phanerochaete chrysosporium P-filter 10.5 42.3C-filter 1.2 37.5

Coriolus versicolor P-filter 11.2 42.8C-filter 2.2 35.8

Phanerochaete sordida P-filter 18.5 53.6C-filter 3.1 39.2

YK – 624

a P-filter = Polycarbonate membrane.C-filter = Cellulose nitrate membrane.

b The original brightness value = 32.6%.c Brown-rot fungus.

Adapted from Kondo et al., 1994.

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by growth of Trametes versicolor in a definedmedium containing formamide; p-xylidineserved to induce laccase production (Kreuterand Rottig, 1990). Laccase from Pleurotusostreatus was active for degradation of phe-nolic compounds, useful in potable water treat-ment (Pickert and Kreuter, 1990). A fungalperoxidase from Coprinus macrorhizus had thecapability to catalyze the removal of toxic or-ganic compounds from waster water, similar tothe function of horseradish peroxidase(AI-Kassim and Taylor, 1994). A peroxidasefrom Coprinus macrorhizus was able to re-move toxic organic compounds from wastewater (AI-Kassim et al., 1994). Screening ofmicrobial exo-enzymes to find a replacementfor horse radish peroxidase in the treatment ofpolluted ground water revealed two Myro-thecium strains, as well as Geotrichumcandidum and Agaricus bisporus with the de-sired qualities. The second organism reducedthe 4-methyl-phenol from 98% to 13% (Shan-non and Bartha, 1989).

When cellulose bleaching effluent wastreated with white-rot fungi, the addition ofglucono-delta-lactone produced a remarkabledecolorization. The effect of glucono-delta-lac-tone was presumed to be associated closelywith the change of pH (Lee et al., 1995). Theefficiency of Coriolus versicolor to decolorizebleached plant waste water was higher whenthe fungus was encapsulated in calcium algi-nate polymer beads, than the cell free system(Pallerla and Chambers, 1995). Of theligninolytic fungi tested, Trametes versicolorwas the most effective microbe to decolorizethe straw soda-pulping effluent (Martin andManzanares, 1994). Manganese peroxidaseseems to play a major role in the initial break-down and decolorization of high molecularweight chlorolignin in bleach plant effluents(Lockner et al., 1991).

In Europe and Scandinavia, a large portionof chemical wood pulp is produced by the sul-fate pulping process, during which most of thewood lignin is partially degraded and dissolvedfrom the cellulose fiber. The residual lignin

(~50 kg metric ton–1 of pulp) is removed invariety of blanching sequences. For example,when a 6-step bleaching and washing processis applied, chlorine, chlorine dioxide, and hy-pochlorite, followed by two alkali extractionsare used (Lindstrom et al., 1981). Chlorinebleaching produces waste steams containinglow concentrations of many chlorinated com-pounds. In the United States, the primarypulping process involves the dissolution of lig-nin from wood at high temperature, using solu-tions of NaOH and Na2S (the Kraft process).Pulps produced by Kraft pulping are in part toremove the residual lignin. White-rot specieswere useful in the degradability of toxic chlo-rinated Kraft bleach mill effluents containinghigh-molecular-weight chlorolignin and low-molecular-weight chlorinated organic com-pounds (Sundman et al., 1980; Eaton et al.,1980; Messner et al., 1990; Archibald et al.,1990a).

Trametes versicolor proved effective indecolorizing and decreasing the toxicity of theKraft bleachery effluent (Roy-Arcand andArchibald, 1991). The intracellular enzymes ofCoriolus versicolor in the form of fungal pel-lets caused a continuous decolorization of bleachKraft effluent. Trametes versicolor effected60% color reduction of pulp and paper industrywaste water in 14 days, in the presence of anadditional carbon source (Purwatl, 1985).Pelurotus sajor-caju effectively removed thecolor from bleach plant effluent when used ina bench scale rotating biological contactor(Kilankaya et al., 1989). A strain Ramaria hadthe highest activity to decolorize waste waterfrom bleaching Kraft pulp; the color removalefficiency was ~90% under air, at a rate com-parable to that attained by Phanerochaetechrysosporium under oxygen. The decoloriza-tion process was monitored through the evolu-tion of molecular weight distribution (decreasein concentration of high molecular weight frac-tion) of chlorolignins in the effluent (Galenoet al., 1990). While using glucose as co-sub-strate, ~90% color reduction of chlorinated lig-nin compounds (from sulfite pulping) was

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achieved by Trametes versicolor within 3 days(Bergbauer et al., 1991). Coriolus versicolorand Pleurotus sajor-caju decolorized the highlycolored Kraft effluents, containing high mo-lecular weight chlorinated oxidized lignin; bothspecies produced 16% 14CO2 from the carbonlabeled bleached Kraft effluent in 20 days(Bourbannais and Paice, 1987).

Chlorinated aromatic hydrocarbons espe-cially chlorinated phenols were removed fromwaste water by polymerization with phenol-oxidizing enzymes from Trametes versicolor(Haars et al., 1988). The white-rot species,Coriolus versicolor decolorized the stable highmolecular weight chromophores released byKraft mill bleacheries. No extracellular peroxi-dases or H2O2 could be detected during decol-orization, although substantial levels of laccase-type phenol oxidases were present (Archibaldet al., 1990a,b).

H. Coal Solubilization

Biological solubilization of low rank coalshas continued to be a subject of interest since1982 (Cohen and Garbriele, 1982), when it wasreported that lignite could be degraded to re-coverable liquid products by Polyporus(Coriolus) versicolor growing in solid agarcultures. Biodegradation of coal (lignite) byPolyporus versicolor was studied to character-ize the products of degradation (Cohen andAronson, 1987). Since then, several white-rotspecies such as Phanerochaete chrysosporium(Scott and Lewis, 1988; Wondrak et al., 1989),Bjerkandera adusta, Poria placenta and Fomesannosus (Wilson et al., 1985) were demon-strated to have this ability of solubilizing coal.Coal solubilization also occurred in cell-freeliquid broths in which the fungi were grown(Cohen et al., 1987, 1989). Extracellular oxi-dases of white-rot fungi transformed low-rankcoal macromolecules and that increased oxy-gen availability in the shallower 10 ml cultures(compared with 15 ml cultures) and favoredcatabolism over polymerization (Ralph et al.,

1996). The purified protein fraction fromCoriolus versicolor contains a syring-aldazineoxidase activity that participates in leonaridite(a highly oxidized low rank coal) bio-solubilization by enzymatic action (Pyne et al.,1987). Other reports (Ward, 1985; Cohen andGabriele, 1982; Dahlberg et al., 1988) also sup-port enzymatic solubilization of coal, whichare influenced by particle size, pH, tempera-ture, concentration of enzymes, and concentra-tion of inorganacious and coal mass (Cohenet al., 1988). Trametes versicolor, Poria pla-centa and Phanerochaete chysosporium wereable to solubilize Australian lignites (Catchesideet al., 1988).

The coal materials such as powdered orhydrogenated hard coal (asphaltene), whenaseptically exposed to the basidiomycete cul-tures resulted in their modification (Bublitzet al., 1994). Trametes versicolor and Phaner-ochaete chrysosporium produced low molecu-lar mass products from biosolubilized coal(Toth-Allen et al., 1994). A basidiomycetestrain, belonging to Aphyllophorales orAgaricales which decomposes coal macromol-ecules, was isolated from humic acid-rich soilof a lignite surface-mining region. The isolateshowed the ability to decolorize liquid darkbrown media containing water soluble coal-derived substances (humic acids). The pres-ence of an easily available substrate is neces-sary for the biodegradation. Solid-state13C-NMR spectroscopy showed an increase ofcarboxylic groups as well as hydroxylated andmethoxylated aliphatic groups, which indicatesan oxidative attack (Wilmann and Fakoussa,1997).

The course of degradation of coal-relatedmodel compounds with the cell-free filtrate ofCoriolus versicolor was phenyl benzoate →benzyl benzoate → benzyl ether → meth-oxybenzophenone. The cell free extract couldnot degrade indole, dibenzothiophene andbibenzyl; however, exposure of these com-pounds to the intact organism resulted in com-plete degradation (Campbell et al., 1988).Leonardite is often found as an overburden to

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lignite deposits and is related to humic acid andis more oxidized than lignites. An extracellularenzyme of the white-rot species Coriolous ver-sicolor caused biosolubilization of leonaridite(Pyne et al., 1988). Products of biological con-version of lignite by Polyporus versicolor areenumerated (Wilson et al., 1987).

Culture volume, growth rate, and the spe-cies under study-white or white-rot variouslyeffected the transformation of solubilized browncoal in liquid cultures (Table 7) (Ralph et al.,1996). Coal solubilizing agent produced byTrametes versicolor was isolated and identi-fied (Cohen et al., 1990). A heat-stable low-molecular-weight (<1000) extracellullar prod-uct in Trametes versicolor cultures was aprinciple factor in the solubilization ofleonardite and other low rank coals (Fredricksonet.al., 1990). Leonardite, was solubilized bythe intact culture, cell-free filtrate and cell freeenzyme of Coriolus versicolor; laccase likeactivity is adduced for this biosolubilization(Campbell et al., 1990).

I. Degradation of Polystyrenes

White-rot species were able to biodegradestyrene (1-phenylethene) graft co-polymers oflignin containing different proportions of lig-nin and polystyrene (Poly 1-phenylethylene).The biodegradation tests were run on lignin/styrene co-polymerization products that con-tained 10.3, 32.3, and 50.4% of lignin, respec-tively. Pleurotus ostreatus, Phanerochaetechrysosporium, and Trametes versicolor de-graded the plastic sample. Both polystyreneand lignin components of the co-polymer werereadily degraded. Scanning electron micros-copy of incubated co-polymers showed a dete-rioration of the plastic surface. The brown-rotfungus Gloeophyllum trabeum did not affectany of these plastics, nor did any of the fungidegrade any of the pure polystyrene. The white-rot species produced and secreted oxidativeenzymes associated with the lignin degradationin liquid media during incubation with ligno-

polystyrene co-polymer. FTIR spectra of theco-polymers also indicated absorbances repre-senting biodegradation of lignin-polystyrene(Milstein et al., 1994a). Production of ligninperoxidases and Mn-peroxidases was observedduring these experiments (Milstein et al., 1992).The white-rot fungus IZU-154 significantlydegraded nylon-66 membrane under ligninolyticconditions. Nuclear magnetic resonance analy-sis showed that four end groups viz. CHO,NHCHO, CH3, and CONH2 were formed in thebiodegraded nylon-66 membranes, suggestingthat nylon-66 was degraded oxidatively. Fur-ther, Phanerochaete chrysosporium (AT CC34541) and Trametes versicolor (IFO 7043)were shown to degrade nylon (Deguchi et al.,1997).

J. Bioremediation of ToxicEnvironmental Pollutants

The white-rot species are unique due to theirproduction of an unusual enzyme system, char-acterized by a special group of peroxidases (Li-p, Mn-p, etc.), that catalyze the degradation oflignin. Advantageously, this ligninolytic enzymesystem displays a high degree of non-specificityand oxidizes a large spectrum of compounds,besides lignin. Among these compounds arenumerous environmental pollutants — toxic or-ganic materials in soils and waters.

1. Chlorinated Organic Compounds

Chlorinated organic compounds such asDDT, lindane, 3,4-dichloroaniline and dield-rin, which are recognized as environmentalhazards were degraded by Phanerochaetechrysosporium (Bumpus and Aust, 1987b;Bumpus et al., 1985; Morgan et al., 1991). Inevery case, a majority of the starting com-pound, if not mineralized, was at least trans-formed (Bumpus and Aust, 1987a). Li-ps wereinvolved in DDT catabolism by Phanerochaetechrysosporium (Bumpus et al., 1985). Miner-

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TA

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alization of DDE to CO2 and a biodegradationpathway for DDT/DDE were investigated byBumpus et al. (1987a,b).

Besides Phanerochaete chrysosporium,with the ability to biodegrade extensively DDT,Pleurotus ostreatus, Phellinus weirii, andPolyporus versicolor also mineralized DDT(Bumpus and Aust, 1987a,b). Pleurotusostreatus and Phanerochaete chrysosporiumwere able to transform 3,4-dichloroaniline(Hallinger et al., 1988). Oxidative dechlorina-tion of aromatic rings of TCP and PCP wascatalyzed by lignin peroxidases (Hammel andTardone, 1988; Mileski et al., 1988; Lin et al.,1990; Venkatadri et al., 1992). Lentinus edodesand Phanerochaete chrysosporium effectedhighest levels of degradation of pentachlorophe-nol in soil at 25°C and pH 4.0; their preferenceof soil moisture was 26 and 47%, respectively(Okeke et al., 1994). Phanerochaete chryso-sporium degraded 2,4-Dichlorophenol by cyclesof oxyreduction and methylation, with a sug-gested pathway involving its oxidative-dechlo-rination to yield 1,2,3,4-tetrahydroxy-benzenethat was then cleaved to produce, after subse-quent oxidation, melonic acid (Valli and Gold,1991). Multiple oxidative dechlorinations cata-lyzed by peroxidases are proposed in thedegradatory pathway of 2,4,5-trichlorophenol.Extracellular protein and mycelium were as-cribed in the degradation of 2,4,6-trichloro-phenol by Phanerochaete chrysosporium(Armenate et al., 1994); the isolation and char-acterization of 1,2,3-trihydroxybenzene, 1,2-dioxygenase from the fungus are reported(Rieble et al., 1994). Polychlorinated dibenzo-p-dioxines recognized as environmental haz-ards due to their acute toxicity to animals andhumans (Schwetz et al., 1973) were mineral-ized by Phanerochaete chrysosporium and theinvolvement of ligninolytic enzymes in theirdegradation is postulated (Hammel et al.,1986a,b; Bumpus et al., 1985; Valli et al.,1992b). Takada et al. (1995) for the first timehave reported the degradation of highly chlori-nated dioxins (40 to 76%) and furans (45 to70%) by Phanerochaete chrysosporium in a

stationary low N medium. Polychlorinated bi-phenyls (extremely unreactive, heat stablechemicals, poor conductors of electricity) suchas aroctor 1,2,5,4, biphenyl, 2-chlorobiphenyl,and 2,2′,4,4′-tetrachlorobiphenyl were miner-alized in the liquid cultures of Phanerochaetechrysosporium (Eaton, 1985; Thomas et al.,1992). Phanerochaete chrysosporium mineral-ized 2,4-di-chlorophenoxy acetic acid (2,4-D)and 2,4,5-trichlorophenoxy acetic acid (2,4,5-T)(Yadav and Reddy, 1993b; Haugland et al.,1990).

Fixed films of Trametes versicolor in rotat-ing tube bioreactors were able to degrade pen-tachlorophenol (Alleman et al., 1995). Pleurotusostreatus, like the white-rot species, degradedtri-two pentachlorinated biphenyls in solid-phase and soil incubation experiments (Zeddelet al., 1994). Trametes versicolor and Pleurotusostreatus degraded TNT in contaminated soils.Primary degradation of more than 90% of theinitial TNT concentration was obtained after 4weeks by both species; Trametes versicolorremoved TNT completely after 6 weeks ofcultivation (Majcherczyk et al., 1994). Severalwhite-rot species, including Phanerochaetechrysosporium, Trametes versicolor, and allthe four species of Ganoderma, removed morethan 50% of the phentachlorophenol (PCP)within 24 hours, although the largest overallreduction of PCP (96%) was achieved byInonotus rickii. Surface area to volume of liq-uid medium was an important factor in theextent of PCP removal (Logan et al., 1994).Nitrogen-limited stationary cultures of thewhite-rot species, Phanerochaetes chryso-sporium, Trametes versicolor and Coriolopsispolyzona mineralized 14C-labeled 3,31,4,41-tetrachlorobiphenyl during a 4-week period(Vyas et al., 1994c).

2. Polycyclic Aromatic Hydrocarbons

Aromatic hydrocarbons are characterizedby the presence of a benzene ring. Polyaromatichydrocarbons (PAHs) are formed during pyro-

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lytic processes or incomplete combustion oforganic substrates; their sources include carexhaust gases, tobacco smoke, and exhaustfumes from industrial and private furnaces.Degradation of benzene, toluene, ethyl ben-zene and xylenes, a group of common organopollutants derived from gasoline and aviationfuels by Phanerochaete chrysosporium, oc-curred under non-ligninolytic culture conditionsin a nitrogen-rich medium. After a 5-day incu-bation, benzene was reduced by 18%, tolueneby 41%, ethyl benzene by 99%, o-xylene by49%, and m-xylene and p-xylene by 67%(Yadav and Reddy, 1993a). In a heterogenoussoil environment, the fungi had different abili-ties to degrade PAH, with Trametes showinglittle or no accumulation of dead-end metabo-lites; Phanerochaete and Pleurotus showedalmost complete conversion of anthracene to 9,10 anthracenedione (Andersson and Henrysson,1996). At least 22 major components fromanthracene oil were degraded by 70 to 100%after 27 days of incubation by Phanerochaetechrysosporium. About 60% of anthracene wasdegraded (after 21 days) in stationary culturesof Phanerochaete chrysosporium, Corioluspolyzona, and Trametes versicolor andPleurotus ostreatus (Vyas et al., 1994b).Phenanthrene degradation may occur underligninolytic as well as non-lignin-olytic conditions of fungal growth (Dhawaleet al., 1992). Hammel (1992) has reviewed themechanism of oxidation of PAHs by Li-p. Sev-eral reports on the role of peroxidases in thedegradation of phenanthrene have appeared(Brodkorb and Legge, 1992; Tatarko andBumpus, 1993; Moen and Hammel, 1994). Thein vitro oxidation of the two polycyclic aromatichydrocarbons anthracene and benzo(a)pyrene,which have ionization potentials of ≤7.45 eV,was catalyzed by laccases from Trametes versi-color. Crude laccase preparations were able tooxidize both anthracene and the potent carcino-gen benzo(a)pyrene. These findings indicate thatlaccase may have a role in the oxidation ofpolycyclic aromatic hydrocarbons by white-rotfungi (Collins et al., 1996). Mixed cultures of

white-rot species such as Dichomitus squalensand Pleurotus species along with soil microor-ganisms enhanced significantly the mineraliza-tion of pyrene (Wiesche et al., 1996).

3. Nitro-Substituted Compounds

Nitro-substituted compounds belong to alarger group of explosive chemicals that alsoencompass nitrate esters and nitroamines alongwith derivatives of chloric acid, perchloric acid,azides, and other compounds. The toxicity andmutagenicity of nitroaromatics and their recal-citrants to biodegradation underlie concernsabout their environmental fate (Kaplan, 1992).Phanerochaetes chrysosporium was able todegrade nitro-arenes. This white-rot species alsodegraded TNT, and RDX (Fernando et al., 1990;Fernando and Aust, 1991; Tsai, 1991; Lebronet al., 1992; Spiker et al., 1992; Michels andGottschalk, 1994). This property has a poten-tial application in the biotreatment of red wa-ter, a hazardous waste stream from explosivemanufacture. An experiment was described inwhich Phanerochaete chrysosporium immobi-lized on a rotating biological contactor wasable to remove 99.5% of TNT at 120 to 175ppm and RDX at 25 ppm from contaminatedwater (Sublett et al., 1992). The rate of TNTand 2-Am DNT and 4-Am DNT reduction cor-related directly with mycelial mass. Toxicitywas inversely related to the amount of fungalhyphae present (Stahl and Aust, 1993a,b). Un-der ligninolytic conditions, Phanerochaetechrysosporium mineralized 2, 4-di-nitrotoluene(Valli et al., 1992a); also this fungus was knownto biodegrade 2,7-dichlorodibenzo-p. dioxin(Valli et al., 1992b). Current lists of the manyxenobiotic compounds degraded by the white-rot species are reviewed (Hammel, 1992; Fieldet al., 1993; Barr and Aust, 1994); mechanismsby which they degrade pollutants are also dis-cussed (Lamer, 1992; Barr and Aust, 1994).The potential for bioremediation of xenobioticcompounds (organic, man-made chemicals) bythe extensively studied white-rot species is re-

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viewed impressively by Pazcznaski andCrawford (1995).

4. Dyes

The dyestuff, textile, paper, and leather in-dustries, which are the major producers andusers of dyes, produce effluents that are usuallyresistant to biological treatments. Glenn andGold (1983) first reported on the decoloriza-tion of several polymeric dyes by Phaner-ochaetes chrysosporium. Dyes such as poly-B-411, poly-R-481, and poly-Y-606 appeared toserve as substrates for ligninolytic enzymes.Remazol Brilliant Blue-R1 (that is similar topoly-B) was decolorized (Ulmer et al., 1984).Color loss of poly-B-411 with lignin degrad-ation was correlated (Chet et al., 1985; Plattet al., 1985). It was also concluded thatno simple relationship existed between thepresence of manganese peroxidase and thedecolorization of the dyes (Freitag and Morrell,1992). Dyes, including crystal violet, pararos-anilyn, Cresol Red, Bromophenol Blue, Ethylviolet, Malachite Green and Brilliant Green(Bumpus and Brock, 1988), were also decol-orized by Phanerochaete chrysosporium.

Cripps et al. (1990) added an entirely newfamily of dyes, the Azo dyes (the largest classof commercially produced dyes not readilydegraded by microbes), to the long list of or-ganic compounds degraded by Phanerochaetechrysosporium. Sulfo- and azo-groups arenot naturally occurring and such dyes are re-calcitrant to biodegradation. Attaching guaiacylsubstituents to azo dyes increased the sus-ceptibility of azo dyes to biodegradation(Paszczynski et al., 1991a,b). Ollikka et al.(1993) found that dyes belonging to four dif-ferent groups (polymeric, azo, heterocyclic, andtriphenyl methane) were decolorized by threemajor lignin peroxidase isoenzymes. Chemicalsteps involved in the degradation of azo dyesby Li-p and Mn-P were elucidated (Goszczynskiet al., 1994; Pasti-Grigsby et al., 1994a).Pycnoporus cynabarinus decolorized the efflu-

ent from a pigment plant, when the waste watersamples were passed through a packed-bedbioreactor. Pasti-Grigs by et al. (1994b) exam-ined a number of azo dyes for their potentialuse as substrates for assaying Li-ps and Mn-psof white-rot species. Involvement of the per-oxidases in the dye degradation is reported byseveral other authors (Capalasch and Sharma,1992; Muralikrishna and Renganathan, 1993;Kling and Neto et al. 1991; Gogna et al., 1991).

5. Other Toxic Compounds

In a report on the metabolism of cyanide,Shah et al. (1991) showed that Phanerochaetechrysosporium was able to mineralize (14C)KCN to 14CO2 and that lignin peroxidase oxi-dized cyanide to cyano radical in the presenceof hydrogen peroxide. The cyanide-containingwaste water can be treated with Pleurotusostreatus, immobilized on a lignin sludge or amixture of sawdust and aerosol (Timofeevaet al., 1989). Kinetics of cyanide binding toperoxidase of Coprinus cinereus was evaluated(Andersen et al., 1991). The degradation ofhydramethylenon (HMN, an amidohydrazonetype insecticide) by Phanerochaetechrysosporium yielded two major breakdownproducts, p-(trifluoromethyl) cinnamic acid andp-(trifluoromethy)-benzoic acid, and a tenta-tive pathway for HMN breakdown was de-scribed (Abernethy and Walker, 1993). Man-ganese enhanced atrazine transformation by thefungus Pleurotus pulmonarius when added to aliquid culture medium at concentrations of upto 300 µm. It is suggested that the stimulationof oxidative activity by Mn might be respon-sible for increasing the biotransformation ofatrazine and for non-specific transformationsof other xenobiotic compounds (Masaphy et al.,1996a). Pleurotus pulmonarius in a mixture ofcotton and wheat straw in SSF, significantlyreduced the added atrazine, due to both adsorp-tion on straw and biodegradation by the mush-room. This process is suggested to be useful todetoxify atrazine (Masaphy et al., 1996b).

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V. BIOSYNTHETIC CAPACITIES

A gross look at the mushroom constituentsindicates that mushrooms have a tremendouscapacity to build their body, composed of aspectrum of carbohydrates, proteins, fats andother substances, unlike green plants, withoutthe requirement for sunlight. They being otherthan autotrophic, depend mainly and directlyon the growth substrates for their derivation ofcarbon, nitrogen and water requirements. Re-tention of their individuality of the species/strain, to synthesize characteristic core con-stituents despite their capacity to grow and yieldon a spectrum of plant wastes obviously reflecton their dramatic ability and potentiality tobiosynthesize their characteristic chemical con-stituents. References are available on such bio-synthetic capacitated enzymes although are notnumerous; however, it is very certain that theoccurrence of the mushroom constituents dif-fering from the growth substrate(s) potentiallyproclaim the biosynthetic capacities of mush-room species. The range of flavor compounds,nucleotides, sterols, amino compounds, sugars,phenolics, and vitamins are illustrative examplesof the diverse capacities of the mushroom spe-cies to biosynthesize. Their biosynthetic ca-pacities in the absence of chlorophyll reflect ontheir marvellous composite action(s) of theenzyme complexes to form the above-listedconstituents.

Action of glycogen phosphorylase in Agari-cus bisporus (Wells et al., 1987), intracellularmycelial proteinases in Flammulina velutipes(Chao and Gruen, 1987), changes in organicacids in Lentinus edodes (Yoshida et al., 1987),changes in low molecular carbohydrates inPleurotus ostreatus (Yoshida et al., 1987a,b),levels of cyclic AMP and adenylate cylase ac-tivity in Lentinus edodes (Takagi et al., 1988),activity of nucleotides in Lentinus edodes(Ohga, 1988), nicotinic and benzoic acids inFavolus ascularis and Flammulina velutipes(Hayashi et al., 1989), chitosan salts in Collybiavelutipes (Yoshikawa, 1988), vegetable oil(Song et al., 1989) and vanillin and ferulic ac-ids in Lentinus edodes (Ikegaya and Goto,

1988), hypoxanthin and inosin compounds inAgroybe cylindracea (Yoshikawa, 1988), in-tracellular glycogen in Coprinus cinereus (Bruntand Moore, 1989), chemicals like brassinolidein Pleurotus sapidus (Feng and Wu, 1990) andtrithiobenzopentathiepin derivatives in Favolusascularius (Sato and Matsuzaki, 1988) in theinduction of fruiting and construction of themushroom fruiting bodies, represent fewglimpses of widely varied synthetic propertiesof mushroom species.

A. Biomass

Biomass production starts once the myce-lium is inoculated to the prepared growth sub-strate. The generated mycelium starts utilizingthe nutrients available in the growth substrate,presupposed by the release and activity ofdegradative enzymes. With the onset of favor-able conditions, the growth cycle culminates inthe production of mushroom fruiting bodies.Biomass includes the mycelium generated inthe growth substrate, developed fruiting bod-ies, and also mycelium grown in liquid cul-tures. The mycelium in growth substrates ismonitored by laccase activity (Turner et al.,1975) or by hexosamine content (Rajarathnam,1981; Plassard et al., 1982) or by ergosterol(Dare et al., 1988; Okeke et al., 1994). Theyield of fruiting bodies on lignocellulosic wastesis expressed as dry weight of the fruiting bod-ies to the dry growth substrate called “Biocon-version efficiency” (BCE), usually expressedas a percentage. Species of Pleurotus have re-corded up to 14% BCE, whereas Agaricus 7%and Volvariella about 3.5% BCE (Rajarathnamet al., 1990). Certain changes have beenrecorded in the constituents of developingfruiting bodies. An increase in dry matterand a decrease in sugars, glycogen, crude fiber,ash, lipids, protein and free amino acids, withincrease in the size of fruiting bodies ofTermitomyces robustus and Lentinus subnudus(Table 8) (Fasidi and Kadiri, 1990) wasobserved. Addition of D-glucosamine-HClor chitosan hydrolysate to the culture of

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TABLE 8Changes in Chemical Constituents a of Termitomyces robustus and Lentinus subnudus duringFruiting Body Development

EthanolMushroom Dry soluble Crude Total Freespecies matter sugars Glycogen fiber Ash lipids Protein amino acids

Termitomyces robustus(pileus)

Mature (6–13 cm) 14.0C 7.9a 6.1a 7.1abc 9.7a 4.6a 16.6a 9.9aYoung (3–6 cm) 14.7bc 6.4b 5.2ab 6.4bc 7.4c 3.9b 13.4b 6.6bVery Young (3 cm) 16.9ac 5.2c 3.0de 5.6c 6.6c 2.6c 10.8c 3.6cLentinus subnudus(pileus)

Mature (4–6 cm) 7.4d 6.5a 8.6a 15.6b 12.0a 3.6a 19.1a 6.9aYoung (2–4 cm) 9.7c 5.1b 7.1b 10.7d 10.6b 2.7b 17.2b 4.5cdVery Young (2 cm) 10.0c 4.8c 6.0c 6.3e 8.6d 2.1cd 15.5c 3.2de

Note: Means followed by the same letter(s) within any mushroom group are not significantly different at P = 0.01 byDuncan’s multiple range test.

a % on dry weight basis.

Adapted from Fasidi Kadiri, 1990.

Lentinus edodes, at the time of inoculation,increased the yield of fruiting bodies by 2.3times that of the control; however, no promot-ing effect was observed when n-acetyl-glucosamine was added to the culture (Terashitaet al., 1993).

Aquatic weeds like Salvinia molesta andEichhornia crassipes resulted in 66 and 57%BCE for Pleurotus sajor-caju (Mani and Philip,1995). A mixture of hazelnut shells, sawdustand wheat bran 1:2:1 resulted in 60% BCE forPleurotus sajor-caju (Ilbay and Okay, 1996).Sugarcane bagasse after pretreatment with so-dium hydroxide (0.5 or 1%) and fermented for5 or 19 days at 80% moisture, with neutraliza-tion by adding gypsum (on 3rd day) resulted inBCE of 147 and 128%, respectively, forPleurotus pulmonarius and Pleurotus ostreatus(Soto-Velazco and Alvarez, 1995). A mixtureof eucalyptus + populus sawdust (40 days) gavethe highest yield (360 g kg–1 dry substrate) forLentinus edodes (Kaur and Lakhanpal, 1995).

Pleurotus ostreatus was able to grow andutilize milk whey as a sole source of carbon

and nitrogen; the fungus accumulated high lev-els of proteins and amino acids (Taratuninaet al., 1988). Organic wastes such as chickenmanure, wheat and cotton straw, and caputz(the solid fraction of digested slurry from ther-mophilic anaerobic digestion of cattle manure)was recycled for mushroom production in Is-rael (Levanon et al., 1988).

Penicillin manufacture waste can be usedfor mushroom culture (Biochemie, 1990). Wastekiselguhr from breweries can be used to pro-duce Pleurotus and Agrocybe schildbach et al.,1992). Barks surpassed woods in contents ofnutrients like nitrogen, total amino acids, re-ducing sugars and starch, which can easily beutilized by Lentinus edodes in the initial stageof growth and formation of the fruiting bodies(Kawachi et al., 1992). Calorimetric measure-ments of barley-straw-grown Pleurotus showedthat energy losses during its life cycle are about35%. Biological efficiency calculated from thespecific energy of products amounts to about23% of the whole process. From 1000 J ofplant input, 231 J builds into Pleurotus fruit

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bodies, of this, 111 J into Pleurotus proteins(Figure 5) (Ginterova and Lazarova, 1989).

“Biomass conversion efficiency” is depen-dent on the occurrence of the contaminants/growth competitors, in the growth substratewhile culturing the mushroom (Rajarathnamet al., 1987a; Gandy, 1985) and several meanshave been advocated to selectively control theweed molds (Rajarathnam et al., 1977, 1979b,1983, 1984, 1992; Zakia Bano et al., 1981),without affecting the mushroom growth andyield; also not to leave any toxic residues in themushroom crop raised. Yield production islargely dependent on the nutritional factors ofthe growth substrate; source and level of nitro-gen in the growth substrate directly influencethe mushroom yield (Rajarathnam et al., 1986;Zakia Bano et al., 1993). Factors governing themushroom production in solid state fermenta-tion are delineated (Zakia Bano et al., 1996).

Sawdust as a substrate for production ofGrifola frondosa (Togashi et al., 1995), mix-ture of eucalyptus wood chips and cotton waste(1:1) + 1% wheat bran for production ofPleurotus ostreatus (Abate, 1995) sugarcanebagasse for growth and yield of Pleurotuscitrinopileatus (Ragunathan et al., 1996) andunfermented cotton waste for production ofVolvariella esculenta (Fasidi, 1996) are enu-merated. Dry maize leaves proved better asgrowth substrate than peanut hulls for Pleurotusostreatus (Bernabe-Gonzalez and Arzeta-Gomez, 1994). Use of mass spectrometry inthe study of functional molecules in mushroomsis reviewed (Sawabe and Okamoto, 1996).

Differential growth and fruiting rate ofnaturally occurring species of Agaricus wereobserved in compost (Alberto, 1995). Maturefruiting bodies of Pleurotus ostreatus var.columbinus grown on hay had significantlyincreased protein content, as a result of in-crease in amino acids such as aspartic acid,arginine, glutamic acid, leucine, lysine andvaline compared with the fruiting bodies grownon wheat straw; neutral detergent fiber, aciddetergent lignin and sugar decreased in theformer (Tshinyangu, 1996). Differences in con-

tents of protein, ether extract, crude fiber, ashand carbohydrates in different parts of mush-room species are presented in Table 9. In gen-eral, protein and ether extract were less in stipecompared with pileus; carbohydrate and ashwere high in stipe, whereas crude fiber contentvaried (Alofe et al., 1996). Improvement of ricestraw quality due to degradation of white-rotswas dependent on species, botanical fraction(leaf or stem) and preparation of substrate priorto inoculation (Karunananda and Varga, 1996).

Mycelium grown in liquid culture is sepa-rated by filtration or centrifugation and ex-pressed as dry weight per liter medium(Rajarathnam and Zakia Bano, 1987a). ThePleurotus ostreatus mycelium grown in the peatextract-based medium was characterized by ahigh protein content, a favorable amino acidcomposition and high concentrations of essen-tial fatty acids and minerals that permit its con-sideration as a potential food compared withfruiting bodies (Manu-Tawaiah and Martin,1987). About 54% crude protein was foundbiosynthesized in the mycelium of Polyporussquamosus, when cultured in a medium ofvinnase (from molasses fermentation) dilutedwith water (1:1) and supplemented with nitro-gen and phosphorus sources (Fidanova andPenev, 1988). Agrocybe aeqerita by growth onorange peel in solid state fermentation increasedits protein content (Rosi et al., 1988). Coriolushirsutus can grow on flax scutch and degrade itto produce the mycelium (in liquid culture) thatcontained about 50% protein (Shcherba et al.,1989). Hydrolysates of peat moss served usefulfor cultivation of single cell protein viz.,Polyporus squamosus and Coriolus species(Stepanov et al., 1990).

B. Carbohydrates

In general, carbohydrates represent the bulkof fruiting bodies accounting for 50 to 65% ondry weight basis. However, starch as such isabsent and glycogen constitutes 8% (ZakiaBano, 1960). Free sugars amount to about 11%,

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FIG

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9.)

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TABLE 9Dry Matter Composition of Pileus and Stipe of Mushroom Species

Lentinus subnudus Psathyrella atroumbonata Termitomyces striatus

Pileus Stipe Pileus Stipe Pileus Stipe

Crude protein 18.54a 9.45 38.94 25.26 30.56 28.79(N × 6.25) 15.80 6.89 36.80 22.71 32.45 26.77

Non-protein 0.54a 0.52 0.65 0.60 1.11 0.96nitrogen 0.60 0.56 0.69 0.61 1.26 0.93

True protein 14.96a 5.01 36.90 20.89 32.16 24.69(N × 6.25) 11.79 3.14 34.00 18.91 28.99 23.00

Ether extract 3.40a 2.54 4.25 3.40 7.05 3.103.21 2.35 4.49 3.67 7.27 3.26

Crude fiber 21.20a 8.90 4.30 10.20 9.90 9.7021.00 8.72 4.08 10.00 9.71 9.69

Ash 11.50a 29.25 18.00 19.20 9.30 15.8011.51 29.00 17.91 18.98 9.10 15.61

Carbohydrate 45.36a 49.85 28.51 32.54 33.69 49.1144.12 48.66 27.65 31.15 33.00 48.56

a Determinations for button and early open-cap stages, respectively.

Adapted from Alofe et al., 1996.

mannitol being the major one (~80% of freesugars) followed by trehalose (the mushroomsugar) and small/trace amounts of glucose.Mannitol may be 30 to 40% on dry weight asin Agaricus bisporus (Rast, 1965; Hammond,1984). In nature, this high concentration ofmannitol aids to maintain the turgor pressure ofthe mushroom cells in the fresh state, aptlyrequired for the discharge of spores produced.Alkali soluble fractions representing hemi-celluloid substances range 5 to 8% (on dryweight) constituted by a heterogenous mixtureof pentoses and hexose sugar(s), and also uronicacids. The alkali insoluble fraction that couldbe hydrolyzed by 72% H2SO4 represents thecelluloid component (35%). Obviously, lack ofreducing sugars and starch, and higher amountsof celluloid substances, including rich dietaryfiber relegate mushrooms as low calorie dietsof high therapeutic value for diabetic patients,to counteract alimentary ulcers and to reduceobesity.

A detailed investigation of the carbohy-drate composition of the fruiting bodies of

Pleurotus flabelatus has been carried out inthis laboratory (Rajarathnam, 1981). The fruit-ing bodies, upon complete acid hydrolysis,showed a total of 57.4% carbohydrates. Matterthat was 70% alcohol soluble contained mainlymannitol and α-α-trehalose, along with traceamounts of glucose. A similarly high level ofmannitol has been reported for Agaricus(Yoshida et al., 1984; Pfyffer and Rast, 1980).α-α-trehalose, due to its common occurrencein mushrooms, has earned for itself the com-mon or trivial name “mushroom sugar”. Thissugar is reported to occur in young mushroomfruiting bodies and is hydrolyzed to glucose asthe mushroom matures (Birch, 1973). In everypart of the fruiting body of Pleurotus ostreatustested, mannitol was higher than glucitol, andmannose and glucose were mainly present inthe stipe region (Kajuno and Miura, 1985).Higher levels of mannitol in mycelium than inthe mushrooms of Lentinus edodes were ob-served; similarly the fruiting body of Agaricusbisporus also contained high levels of mannitol(Tan and Moore, 1994). Yoshida and colleagues

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(1986) have studied the changes in distributionof low molecular weight carbohydrates andpolysaccharides in the fruiting bodies ofPleurotus ostreatus. Trehalose and mannitolfound in major quantities are supposed to func-tion as the main translocate carbohydrates.

Sugar composition in the fruiting bodies ofLentinus edodes, Lyophyllum shimeji, Pleurotussajor-caju, and Volvariella volvacea reflectedthat β-glucans were the major fiber polysac-charide with chitin, hemicelluloses, andpolyuronides as minor constituents (Cheung,1996). Fruiting bodies of Lyopyllum shimejicontained ~30% crude protein and ~57% car-bohydrates on dry basis; trehalose was the majorfree sugar accounting to 12% on dry weight(Yoshida and Fujimoto, 1994).

In the fruiting bodies of Agaricus bisporus,D-mannitol contributes up to 40% of the dryweight, with the synthesis of the polyol occur-ring by reduction of D-fructose in an NADPH-dependent dehydrogenase reaction, and iscoupled to the dehydrogenase reactions of thehexose monophosphate shunt (Rast, 1965). Sig-nificant changes were observed to occur incarbohydrate metabolism during the initiationand development of fruiting primordia in Agari-cus bisporus (Hammond, 1984). Mannitol waspresent at low concentrations in the mushroommycelium, but increased dramatically (30 to50% of dry weight) in differentiating fruitingbodies. The enzyme mannitol dehydrogenasecatalyzes mannitol synthesis from fructose us-ing NADPH as a co-factor (Edmundowicz andWriston, 1963). Increases in mannitol synthe-sis and glucose-6-phosphate dehydrogenaseactivity were related to the initiation and devel-opment of Agaricus fruiting bodies (Hammond,1981). Activities of mannitol dehydrogenaseand fructose-6-phosphatase were high in theearly stages of development and reached amaximum during the later stages of develop-ment respectively, ultimately dropping to a lowlevel after sporulation (Morton et al., 1985). InAgaricus bisporus, mannitol-1-phosphate de-hydrogenase was not detected (Hault et al.,1980), as in Lentinus edodes (Kulkarni, 1990).

The pathway of mannitol synthesis in Lentinusedodes appears to utilize fructose as an inter-mediate.

Thus, the carbohydrates of mushrooms aremainly structural, excepting the free sugar com-ponents required to maintain high osmotic con-centration and to serve for the energy releaserequired in pace with the fast rate of metabo-lism of fresh mushrooms. The glucose metabo-lism is prominent, nevertheless with smalleramounts of pentoses complexing the core struc-ture. Enzymes aimed at their syntheses charac-terize the carbohydrate constituents and thus,species/varietal variations are legitimate. It isimportant to mention at this juncture that it isthe glucosamine synthetase which serves tobuild up the middle lamella of cell walls. Oftenfor this reason, follow up of the glucosaminecontent and eventually its enzyme of synthesiswould serve to trace the extent of biomass pro-duction in solid state fermentation.

C. Amino Acids, Peptides, andProteins

Nitrogen compounds in the amino form asamino acids, peptides, and proteins representthe second major fraction of mushrooms nextto carbohydrates. About 20% amino acids (AA)are in the free form (Table 10), while the restrepresent the proteins. Several references aregiven to illustrate the amino content of mush-rooms, their quality and predicted nutritionalvalue (Crison and Sands, 1978; Rajarathnamand Zakia Bano, 1991; Buswell and Chang,1993). What is more significant from the bio-logical point is the capacity of mushrooms toobtain their nitrogen solely from the growthsubstrates, and to synthesize and transform theamino substances according to the genetic codedecided by the heritable matter. In this regard,mushrooms of Pleurotus type deserve specialattention, as they can virtually grow directly onnatural lignocellulosic wastes of very low ni-trogen content, obviously concentrating intotheir biomass of nitrogen content higher than

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TABLE 10Free Amino Acids in Mushroom Species (g per 100 g)

Boletaceae

Boletus Boletus Boletus Leccinum Suillus Suilluscalopus reqius sardous quercinum granulatus luteus

Glycine 4.9 4.2 3.1 2.9 3.8 2.9Alanine 5.6 6.0 5.3 4.0 4.8 3.6Beta- 0.4 0.5 — tr — 0.2AlanineValine 8.3 10.0 8.5 12.8 5.8 7.7Isoleucine 5.6 3.5 4.5 4.7 3.2 3.9Leucine 7.6 5.2 5.8 6.3 7.5 5.9Threonine 3.8 4.1 5.0 4.3 3.7 2.8Proline 9.5 14.5 10.3 15.2 12.5 15.1Serine 7.9 9.2 12.1 13.0 9.3 11.0Cystine 1.0 1.5 1.3 1.6 1.2 1.4Asparginea 6.7 8.6 8.2 5.6 6.7 8.3Phenylala- 1.9 0.9 1.5 2.5 2.4 1.6nineGlutaminea 11.4 12.0 11.5 9.9 14.9 12.8Lysine 6.3 4.8 4.2 4.9 4.5 4.2Methionine 1.2 0.5 0.9 1.3 0.9 1.5

Cortinariaceae Hydnaceae Polyporaceae Russulaceae

Cortinarius Hydnum Polyporus Russula Russulalargus norensis repandum pes-caprae cyanoxantha xerampelina

Glycine 2.1 1.6 2.9 1.5 2.3Alanine 2.4 4.4 3.3 3.9 5.8Beta- tr — — tr —AlanineValine 13.8 10.5 12.3 14.6 15.1Isoleucine 4.9 4.6 5.7 2.3 4.7Leucine 6.3 2.6 3.9 6.4 5.5Threonine 4.3 2.2 3.4 3.5 4.0Proline 17.2 20.1 12.0 16.0 12.5Serine 11.0 13.4 10.7 15.2 14.9Cystine 1.7 0.7 0.5 0.5 0.8Asparginea 6.6 10.4 8.6 6.8 3.7Phenylala- 3.0 3.8 4.5 1.4 0.8nineGlutaminea 10.3 9.8 11.1 11.3 10.5Lysine 5.1 3.0 5.2 3.9 2.8Methionine 1.0 0.5 1.0 0.2 0.3

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TABLE 10 (continued)Free Amino Acids in Mushroom Species (g per 100 g)

Boletaceae

Boletus Boletus Boletus Leccinum Suillus Suilluscalopus reqius sardous quercinum granulatus luteus

Tyrosine 0.5 0.3 1.2 0.8 1.6 1.0L-Dopa 3.0 3.8 3.5 2.5 4.1 3.5Histidine 2.5 3.3 4.1 2.9 2.2 3.5Arginine 3.8 1.1 2.1 2.0 4.3 2.4Tryptophan 1.4 0.9 1.8 0.5 1.7 1.5OH-Pro- tr 0.5 tr 0.3 — —Hydroxypro-line

Unidentified 6.7 4.6 5.0 2.0 4.9 5.2

Note: tr = Trace amounts.— = not detected.

a Values for Aspartic acid and Glutamic acid include asparagine and glutamine. Each value is the mean of fivereplicates.

Cortinariaceae Hydnaceae Polyporaceae Russulaceae

Cortinarius Hydnum Polyporus Russula Russulalargus norensis repandum pes-caprae cyanoxantha xerampelina

Tyrosine 0.6 0.9 1.3 0.8 1.4L-Dopa 2.2 2.9 2.7 2.1 3.6Histidine 2.0 0.9 1.3 2.1 3.5Argenine 1.4 2.8 4.4 1.9 2.5Tryptophan 0.7 1.1 1.5 1.8 1.4OH-Pro- 0.6 — 0.5 tr 0.3Hydroxy-proline

Unidentified 2.8 3.8 3.2 4.6 3.5

Adapted from Senatore et al., 1988.

the growth substrate. Ginterova and Lazarova(1987) have studied a possible balance of theamino compounds in the growth substrate, rela-tive to the mushroom crop harvested, to con-clude that certain strains of Pleurotus as eu-karyotes do possess the property of fixingatmospheric nitrogen. Whatever the case, thismuch is certain, the quality of mushroom pro-teins and their essential amino acid spectrum(Table 11) have elevated the rank of mush-rooms among the class of other nutritionallyimportant food materials. Therefore, mush-

rooms have been aptly recommended by theFAO as supplementary foods to the growingpopulations of developing countries, whichdepend mainly on a cereal diet. They would bevaluable supplements to most of the EAA andcan aid in overcoming overall protein defi-ciency (Zakia Bano and Rajarathnam, 1982).

This takes us to a consideration of theprimary amination, and glutamic acid concen-trations in mushrooms. Subsequent transami-nases, serve to make up the net spectrum ofamino acids and proteins. It is vital to stress the

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TABLE 11Essential Amino Acid Composition of Mushroom Species

Pleurotus Pleurotus Pleurotus Agaricus Volvariella Lentinus Hen’sAmino acids a florida sajor-ca ju ostreatus bisporus diplasia edodes eggb

Leucine 7.5 7.0 6.8 7.5 5.0 7.9 8.8Isoleucine 5.2 4.4 4.2 4.5 7.8 4.9 6.6Valine 6.9 5.3 5.1 2.5 9.7 3.7 7.3Tryptophan 1.1 1.2 1.3 2.0 1.5 nd 1.6Lysine 9.9 5.7 4.5 9.1 6.1 3.9 6.4Threonine 6.1 5.0 4.6 5.5 6.0 5.9 5.1Phenylalanine 3.5 5.0 3.7 4.2 7.0 5.9 5.8Tyrosine 2.7 6.3 3.0 3.8 2.2 3.9 4.2Cystine 0.2 1.2 0.4 1.0 3.2 nd 2.4Methionine 3.0 1.8 1.5 0.9 1.2 1.9 3.1Arginine 3.2 6.2 5.3 12.1 8.3 7.9 6.5Histidine 2.8 2.2 1.7 2.7 4.2 1.9 2.4Total essential 46.4 43.4 35.5 41.6 50.1 38.4 51.3amino acids(excluding)arginine andhistidine)

Note: nd = not determined.

a g of amino acid per 100 g of corrected crude protein.b For comparison.

Adapted from Zakia Bano and Rajarathnam, 1982.

capacity of these specialized fungi to secreteand operate a spectrum of aminases to bringout a carbon copy of the parental cell compo-sition for amino substances. As the geneticconstitution is mostly other than the diploidstate, there is always a possibility to introducevariations in the operation systems, at the hit ofenvironmental factors (physical, chemical, orbiological), that might answer the question ofgenesis of variability whether desirable or not,over a course of their repeated culturing pass-ing through several life cycles and sub-culturings.

As fats and carbohydrates are rarely lack-ing in a diet, protein constitutes the most criti-cal component contributing to the nutritionalvalue of the food. The crude protein content ofmost of the foods is calculated from their nitro-gen content, using the conversion factor 6.25,based on the presumption that most of the pro-

teins contain 16% nitrogen (N) and taking intoaccount that they are nearly 100% digestibleand that negligible amounts of non-protein ni-trogen are present. Studies of crude mushroomprotein, however, suggest that only 34 to 89%of the protein (N × 6.25) is digestible. Addi-tional workers have indicated a probable di-gestibility of 60 to 70% of the mushroom pro-tein. This reduced coefficient of digestibilitycan be partially explained by the fact that mush-rooms contain a significant amount of non-protein nitrogen in the form of glucosamine intheir chitinous cell wall; nitrogen would becalculated as crude protein after standard nitro-gen analysis. A closer approximation of mush-room protein content can be obtained by usinga conversion factor equal to (70%N × 6.25), i.e.(N × 4.38). Although this corrected crude pro-tein factor may not be accurate for all of thespecies of mushrooms and may appear high in

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the light of the low co-efficient of digestibilitydetermined by some investigators, this factorhas been adopted for mushrooms in severalfood composition tables (FAO, 1970; FAO/WHO, 1972; Leung et al., 1972). To compoundthe confusion concerning mushroom protein,Fitzpatrick et al. (1946) found that a purifiedmushroom protein isolate contained 11.79% Nrather than the expected 16%. Based on theirdata, a conversion factor of (N × 8.48) wouldbe more appropriate for estimating mushroomprotein if the nitrogen content of the chitin andfree amino acids could be ignored. Relativeamounts of non-protein N and protein N in

several mushroom species are indicted(Table 12). The problems encountered in de-termination of true protein content, excludingall other non-protein nitrogenous substances,in Agaricus bisporus are critically evaluated(Braaksma and Schaap, 1996). The proteincontent of Pleurotus ostreatus calculatedfrom the non-chitinous nitrogen content usingthe factor 6.58 was 17.1 and 23.5% dry weightof fruiting bodies on wheat straw and grasshay, respectively, rather than 18.4 and 24.4%(as total nitrogen × 6.25) (Tshinyangu andHennebert, 1996). Analyzing 13 species ofmushrooms, it was found that the distribution

TABLE 12Total Protein and Non-Protein Nitrogen Contents ofMushroom Species

Total N Protein N Non-Protein N(% of dry

Species wt.) (% of Total N)

Agaricus 5.0 63 37bisporus

Boletus 6.4 69 31badius

Boletus 6.4 71 29edulis

Canthrellus 3.6 67 33cibarius

Gyromitra 5.0 70 30esculenta

Lactarius 4.0 57 43vellereus

Leccinum 5.6 72 28scabrum

Lepiota 7.0 47 53procera

Paxillus 4.2 66 34involutus

Pleurotus 3.6 70 30ostreatus

Suillus 4.3 61 39bovinus

Suillus 5.1 77 23luteus

Tricholoma 2.6 62 38equestre

Tricholoma 8.8 43 57nudum

Adapted from Kurkela et al., 1980.

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of protein N averaged 67% to total N; averageN to protein conversion factor was 5.99(Fujihara et al., 1995). Heteroglycan orheteroglycan-protein complexes isolated fromthe mycelium of Grifola frondosa reduced tu-mor growth by activating the immune systemas a biological response modifier (Zhung et al.,1994). Different kinds of protein (crude, di-gestible, and nondigestible) were analyzed incap and stipe of Pleurotus ostreatus in fourstages of development; both the cap and stipehad high digestible protein that averaged to92% (Vetter and Romoczi, 1993). During de-velopment of white button mushrooms, solubletrue protein content showed higher levels dur-ing the early stages of growth indicating thathigher levels of protein are required for thedifferentiation of mycelium. The non-proteinnitrogenous compound content increasedsharply at the open and flat stages indicatingthat non-protein nitrogenous compounds con-tribute largely to the increased crude proteincontent (Surinder Kumar et al., 1993). About40% of the total N content of dry mushroomswas found to be contributed by protein aminoacids; the digestibility of mushroom crude pro-tein being 79% compared with 100% for anideal protein (Friedmann, 1996). The relativedistribution of nitrogenous components inmushrooms is compared with other majorgroups of foods (Sosulski and Imafidon, 1990).

The non-protein nitrogen compounds, mostsignificant in this respect are free amino acids(FAA), chitin, nucleic acids and urea; how-ever, urea has only a limited occurrence in thehigher fungi. In addition to these compounds,nucleotides and related compounds, ammonia,several kinds of amines and quartenary ammo-nium compounds, volatile nitrogen compounds(other than amines) and nitrogen-containingvitamins are found in the higher fungi. Theoccurrence of non-protein amino acids in mush-room species is presented (Table 13).

At least 20% of the amino N was repre-sented in the form of FAA; values ranged up to40% of dry weight (Stankeviciene and Urbonas,1991). By far, glutamic acid is the most abun-

dant amino acid (AA) both among the free andbound AA followed by others like threonine,valine, alanine and aspartic acid (Abou-heilahet al., 1987; Senatore, 1990; Hayakawa et al.,1991; Surinrut et al., 1987; Terashita et al.,1990). Analyzing the fruiting bodies of 113kinds of mushrooms for their amino acid con-tents, the average of total free amino acids was213 mol g–1 dry matter. It was found that theamount of alanine, glutamic acid and glutaminewas very high and they were the dominantamino acids in the free amino acid pool. Con-tents of non-protein amino acids were com-monly low, but ornithine, γ-amino-n-butyricacid and cystathionine were proven to be widelydistributed in the mushrooms. As far as thepresent survey could determine, there seems tobe no obvious correlation between the freeamino acid pool and taxonomic groups ofmushrooms (Sato et al., 1985). Both Volvariellavolvacea and Ganoderma lucidum fruiting bod-ies serve as a good source of phenylalanine andtyrosine, tryptophan and valine (Sornpraset,1995). In the fruiting bodies of Tricholomagiganteum, aspartic acid and alanine were themost abundant constitutive AA; aspartic andglutamic acids were dominant among FAA(Fujita et al., 1990). Agaricus bisporus con-tained 37.66% protein, which contained 19 AAincluding all the essential ones (Stankevicieneand Urbonas, 1988). Alanine, proline, serine,and valine were determined to be the abundantAA in five mushroom species (Senatore, 1992).Extracts of mushrooms in boiling water con-tained significant quantities of AA (Liu andGan, 1987). By exposure of Lentinus edodes,Flammulina velutipes and Grifola frondosa tosunlight or UV irradiation for 3 h, the amountsof FAA increased; sweet tasting AA increased,while bitter tasting AA decreased (Kiribuchi,1991). With increased differentiation and ma-turity in the fruiting bodies of Agrocybecylindracea, asparatic acid, threonine, serine,alanine and tyrosine decreased, whereas lysineand arginine slightly increased (Tabata andYamasaki, 1995). Essential amino acids (EAA)are made up to 44 to 50% of total amino acids

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TABLE 13Non-Protein Amino Acids of Mushroom Species

Amino acid Species

Agaritine (β-N-(g-L(+)- Agaricus bisporusglutamyl)-4-hydroxymethylphenylhydrazine)

L-2-Amino-4-Chloro-4- Amanita pseudoprophyriapentenoic acid

L-2-Amino-3-formyl-3- Bankera fuligineoalbapentenoic acid

L-2-Amino-3-hydroxy- Tricholomopsis rutilanshex-4-ynoic acid

L-2-Amino-3-hydroxy- Bankera fuligineoalbamethyl-3-pentenoic acid

β-Aminoisobutyric acid Agaricus bisporusL-2-Amino-4-methyl-5- Boletus sp.hexenoic acid

L-2-Amino-4-methylpimelic Lactarius guietusacid

Cis-3-Amino-L-proline Several Morchella speciesL-3-(3-Carboxyfuran-4-yl) Phyllotopsis nidulansalanine

Citrulline Tricholomopsis rutilansα-β-Diaminopimelic acid Boletus edulis2,4-Diaminobutyric acid Agaricus bisporusN-Ethyl-γ-glutamine Boletus edulisHomoserine Agricus bisporusN-γ-L(+)-Glutamyl-P- Xerocomus badiushydroxyaniline Agaricus bisporus5-Hydroxytryptophan Agaricus hortensisKynurenine Inocybe species2-Methylenecyclopheptene- Agaricus bisporus1,3,-diglycine Lactarius helvus

β-Methylene-l-(+)-norvaline Lactarius helvusβ-Nitraminoalanine Agaricus silvaticusOrnithine Several speciesPipecolic acid Several speciesSarcosine Agaricus bisporus

Adapted from Kurkela et al., 1980.

(TAA) depending on the age and species, withregard to the data on Agaricus bisporus,Armillaria mellea, Kuehneromyces mutabilis,Macrolepiota procera, and Macrolepiotarhacodes (Stankeviciene and Urbonas, 1991).Both Agaricus bisporus and Pleurotus ostreatuswere poor sources of sulfur containing AA(Stancher et al., 1990).

At four different stages of development inAgaricus bisporus, highest amounts of EAA

and TAA were in the caps compared withall other stages of stipes/caps (Bakowskiand Kosson, 1985). The trend was quitepeculiar in Pleurotus sajor-caju; the AA con-tents decreased with increase in size of fruit-ing bodies during growth and development(Chen et al., 1987). The protein content alsodecreased with the enlargement of the fruitingbody in Pleurotus citrinopileatus (Ghosh et al.,1991).

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Of the FAA estimated in the mycelium inthe species of Lentinus and Collybia, methion-ine was high in the former (Roy and Samajpati,1988). Aspartic acid, glutamic acid, alanine,leucine, valine and tyrosine were the major AAin the cultured mycelium of Pleurotus ostreatus(Aoyama, 1989). Three new AA viz., valino-pine, epileucinopine, and isoleucinopine wereisolated from the toxic mushroom Clitocybeacromelalga (Fushiya et al., 1994).

Glutamate containing dipeptide fromClitocybe acromelalga and polypeptide com-plex from Coriolus versicolor were isolated(Yamano and Shirahama, 1994; Yang et al.,1995). Copper binding peptide purified fromGrifola frondosa enhanced intestinal absorp-tion of copper (Shimaoka et al., 1994).

Coprinus psychromorbidus exhibited tem-perature induced synthesis and accumulationof sclerotial polypeptides in vegetative phase(Newsted and Huner, 1988). The major polypep-tides associated with such a differentiation(Sclerotia development) were characterized bytheir electrophoretic nature; the isoelectric pointranged from 7.0 to 7.7 (Newsted and Huner,1987). A glycopeptide (molecular weight 105daltons) was prepared from the ethanolic ex-tracts of mycelium of Lentinus edodes possess-ing anti-tumor and immuno-stimulant activi-ties (Yang, 1989).

Four proteins of molecular weights 74,000,72,000, 70,000, and 68,000 were identified andpurified from Coprinus cinereus; the proteinswere abundant in the cap cells (Kanda et al.,1986). A glycoprotein (2.5 to 3.0%) from themycelium of Dictyophora duplicata was sepa-rated (Li et al., 1988).

Two DNA binding proteins (designated asLE1 and LE2) were purified from Lentinusedodes; their molecular weights were estimatedto be 58,000 and 42,000, respectively. LE1 hada maximum DNA-binding activity at pH 3.5 to4.0, whereas LE2 was active at pH 3.5 to 10.0.LE2 enhanced topoisomerase activity underappropriate conditions (Habuka et al., 1991). Aubiquitin immuno-reactive protein with a mo-lecular weight of 27,800 daltons, present mainly

in the cap of young fruiting bodies of Coprinuscinereus, was isolated and its amino-terminalsequence determined (Kanda et al., 1990).

Glycoproteins isolated from Volvariellavolvacea at 5 mg kg–1 showed 100% control ofSarcoma-180 in mice (Misaki and Sone, 1987).A polysaccharide-peptide produced by themycelium of Lentinus edodes containing Fe,Zn, Cu, Co, and Ni was found to be a neoplasminhibitor (Ren et al., 1990). Collagen bindingprotein (hitherto undescribed fungus protein)was isolated from the mushroom, Hypsiziqusmarmoneus, that can interact with animal ex-tracellular matrix proteins (Tsuchida et al.,1995).

The soluble mushroom proteins were dem-onstrated to be dimers, trimers and decamers ofthe simple, main protein (polypeptide) with amolecular weight 15,000 (Miletic et al., 1990).Water soluble proteins of Boletus edulis, Bol-etus chrysenteron, Boletus scaber and Collybiaradicata were investigated for their electro-phoretic characterization (Miletic et al., 1988).

Buffer (pH = 7.8) extracts of Grifolafrondosa and Pleurotus ostreatus yielded cop-per containing proteins, useful as metal carriersin intestinal absorption (Shimaoka et al., 1990).Studies of the free and protein AA compositionof oyster mushrooms (Pleurotus florida,Pleurotus ostreatus, Pleurotus sajor-caju) re-vealed appreciable amounts of all EAAs, withthe exception of tryptophan, which was notpresent in a free form and comprised 0.53 to0.61 g per 100 g of protein. The proteins con-tained ~30% of aspartic acid, glutamic acid andleucine, whereby EAAs, accounted for 51% ofthe total (Eder and Wuensch, 1991).

Protein AA in the non-protein N, and pro-tein N fractions accounted for about 65% of thetotal N, suggesting that a practical N-proteinconversion factor for the mushrooms may beconsidered to be, on the average, about 4(Ogawa et al., 1987). Interference of non-pro-teinaceous N compounds while determining AAand protein contents of Canthrellus cybariusare discussed (Danell and Eaker, 1992). Theextracted protein was 74-80% of the total

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organic N, in Boletus tropicus and 53.61% inBoletus granulatus (Pecora, 1989). Purifica-tion of proteins from Pleurotus cornucopiaeand the levels of albumins, globulins, prola-mins, and glutelins and their AA compositionof Coriolus hirsutus were studied (Min et al.,1988; Babitaskaya et al., 1989a). A toxic pro-tein (Bolesatine) from Boletus satanus inhib-ited synthesis of globulin by a rabbit reticulo-cyte lysate preparation (Kretz et al., 1989).

D. Lipids

Dry mushrooms contain about 3% fat, pre-dominated (>75%) by the unsaturated fattyacids — linoleic and linoleinic acids. Stearic,oleic, and palmitic acids contribute to the mainsaturated fatty acids. Sterols useful for the hu-man body are present. The spectrum of fattysubstances present in mushrooms unequivo-cally support their ability to form the fatty ac-ids, and it is important to remember that thelignocellulosic growth substrates on which theyare grown barely contain any fat. The operationof lipoxygenases, but more strongly the fastrate of cell multiplication during fructification,add further support to the active lipid metabo-lism in the mushroom cells as it is well knownthat phospholipids presuppose the formation ofcell membranes/walls. Thus, the quality ofmushroom fat is very suitable for human health,and prone to the least risk of atherosclerosis.

The crude fat of mushroom includes, ingeneral, representatives of all classes of lipidcompounds, namely free fatty acids, mono-,di-, and triglycerides, sterols, sterol esters, andphospholipids. The major neutral lipid ofPleurotus ostreatus is a triglyceride and consti-tutes 29% of the dry weight (Hasan et al., 1965).The major fatty acid is linoleic acid (79.4%),which occurs along with lesser amounts ofpalmitic (14.3%) and linoleinic acids (6.3%).Squalene ergosterol (free and esterified) andubiquinone 7 have also been investigated inorder to find out their general properties, toidentify the fatty acid compounds, and to deter-

mine characteristics of unsaponifiable matter(Yokokawa and Mitsuhashi, 1981). It is worthnoting that similarly high concentrations ofpalmitic, stearic, oleic, and linoleic acids havebeen observed in Agaricus bisporus along witha large number of free and combined fatty ac-ids (Hughes, 1962; Holtz and Schister, 1971).

The fruiting bodies Pleurotus florida werefound to contain 6% of total lipids on a dryweight basis. Major fractions of total lipidsoccurred as free and non-volatile lipids. Frac-tionation studies of the total lipids indicated thepresence of triglycerides (61.4%) and phos-photidyl choline (55.3%) as the major compo-nents of non-polar and polar lipids, respec-tively. GLC analysis of the fatty acids hasrevealed that unsaturated fatty acids of C:18class accounted for a major fraction. Linoleicacid (18:2) was found to be the main unsatur-ated fatty acid, comprising 72.8% of the totalacid. Palmitic acid (16:0) was the major satu-rated fatty acid; unusual and branched fattyacids were not detected. Hader and Cohen-Arazi (1986) have also observed similarly highvalues for palmitic and linoleic acids in thefruiting bodies of Pleurotus ostreatus grownon cotton straw. Solomko et al. (1984) havefound that fruiting bodies of Pleurotus ostreatuscontain free fatty acids of 5 to 20 carbon atoms,linoleic acid (~56%) being the predominantone. Kwon and Uhm (1984) also observed thepredominance of linoleic acid in Pleurotusostreatus and Pleurotus florida. Sterols foundin mushrooms act as provitamins and the highlevels of linoleic acid among the fatty acidsplays an important nutritional role (Willemot,1980; Bronsgeest-Schoute et al., 1981;Antonone et al., 1985). In the several mush-room species studied, ergosterol was predomi-nant of the sterols. The composite fatty acids ofseveral mushroom species were determined bySenatore et al. (1988) (Table 14).

Cap and stalk of Lentinus edodes containedfat at 4.58 and 2.65% levels, respectively. Themajor neutral lipid was triglycerides, followedby sterol esters, sterols, diglycerides andmonoglycerides. Linoleic, palmitic, and oleic

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TABLE 14Fatty Acids of Basidiomycetes (mg g –1)

Fatty acids

Species C10:0 C12:0 C14:0 C14:1 C15:0 C16:0 C16:1 C17:0

Boletus calopus tr — 4 — — 151 5 —Boletus reqiustr tr 2 tr — — 190 3 —Boletus sardous — 4 3 — — 186 3 —Leccinum 2 3 10 tr 2 165 9 trquercinum

Suillus tr 2 tr — tr 177 4 —granulatus

Suillus luteus — tr 3 tr tr 157 6 trCortinarius tr tr 5 — tr 211 16 —largus—norensis

Hydnum repandum tr 3 — 8 — 158 tr 26Polyporus — 4 7 tr — 202 20 —pescaprae

Russula — 5 tr tr — 172 11 trcyanoxantha

Russula xerampelina — 6 tr — 2 191 14 —

Fatty acids

Species C18:0 C18:1 C18:2 C18:3 C20:0 C22:0 C24:0 Unidentified

Boletus calopus 81 213 501 8 tr — — 37Boletus reqius 42 174 546 13 — 30Boletus sardous 51 150 558 15 tr — — 30Leccinum 116 126 524 13 tr — — 30quercinum

Suillus 65 148 563 9 tr — — 32granulatus

Suillus luteus 46 190 545 20 — — — 33Cortinarius 53 218 469 3 tr — — 25largus—norensis

Hydnum repandum 60 192 487 35 — 2 tr 29Polyporus 40 282 403 3 — 5 3 31pescaprae

Russula 47 260 474 3 — — — 28cyanoxantha

Russula 45 205 505 tr — — — 32xerampelina

Note: tr = Trace, less than 1.0 mg g–1.— = Not detected.Each Value is the mean of five replicates.

Adapted from Senatore et al., 1988

acids were the major fatty acids. The effect ofdrying on lipid fractions and fatty acid contentsis discussed (Haraguchi, 1986). The lipid com-position of Auricularia polytricha indicated thepossible capacities of the mushroom to form

and contain lipid constituents in its fruitingbodies. Here, the dried mushroom containedabout 1.47% lipid. Total lipid of fresh mush-rooms consisted of 61% neutral lipid, 24.1%phospholipid and 14.9% glycolipid. In the neu-

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tral lipid, phospholipid, and glycolipid frac-tions, triglyceride, phosphatidyl-choline andcerebroside were predominant, respectively.The major fatty acids of these lipids were C18:2,C18:1 and C16 (Takenaga et al., 1988). Dis-cussed in the review by Hiroi (1988) is thechemotaxonomy of basidiomycetes based onthe fatty acid composition of fruiting bodiesand basidiospores, and on mushroom specificacids, 6-oxo-octadecanoic acid and dehydro-crepenynic acid. The high degree of unsatur-ated fatty acids and contents of phospholipidsindicated a high biological value of myceliallipids by Flammulina velutipes and severalstrains of Basidiomycetes (Kapich et al., 1989).New types of glycosyl phosphosphingolipidsin Hypsizigus marmoreus and Pleurotuscitrinopileatus were determined by fast atombombardment mass spectrometry (Sawabe etel., 1996). Exposure of developing fruitingbodies of Pholiota nameko to ozone decreasedthe linoleic acid content and PUFA/SFA ratioin the pileus, stipes and entire fruiting body(Watanabe et al., 1994). Linoleic and palmiticacids were the major constituents of the freeand bound fatty acid fractions of cream andwhite varieties of Agaricus bisporus andPleurotus ostreatus; free fatty acids predomi-nated over bound fatty acids in Agaricusbisporus but not in Pleurotus ostreatus(Stancher et al., 1992a). The major fatty acidsin Agaricus bisporus were linoleic (C18:2) 68.4to 69.3, palmitic (C16:0) 14.8 to 15.2 and stearicacid (C18:0) 4.4 to 4.5%. C8, C15, and C17were present in greater amounts in the whitecultivar; C12 and oleic acid (C18:1) were moreabundant in the cream cultivar. Major fattyacids in Pleurotus ostreatus were (C18:2) ~59.4,(C16:0) ~21.5, and (C18:1) ~9.8% (Stancheret al., 1992b).

The structure of a novel fatty acid (9R,10S, 12Z)-9, 10-dihydroxy-8-oxo-12 octade-canoic acid isolated from the mushroomHericium erinaceum is elucidated. The fattyacid showed cytotoxicity against Hela cells andinhibitory activity on tea pollen growth(Kawagishi et al., 1990a). Bisaria et al. (1990)

have studied the biological importance of sev-eral of the white and white-rot agents ofAphyllophorales and Agaricales in forming highlevels of linoleic acid (in the mycelium grownon shaken media containing 30 g glucose L–1

and C:N ratio at 27:1). Supercritical fluid ex-traction of fatty acids from Agaricus species isaccounted by Lu and Li (1988). The main fattyacids from the fruiting bodies of Flammulinavelutipes were 18:2n6, 18:3n3, and 16:0(Takenaga et al., 1995).

The biosynthesis of lipids in the myceliumand fruiting body of Pleurotus sajor-caju wasstudied. Whereas in the mycelium, the biosyn-thesis of lipids was directed primarily towardstorage (e.g., tri-acylglycerols), in the fruitingbody it was directed toward structural compo-nents (e.g., sterols). The incorporation of 14Cprecursors into non-polar and polar lipid frac-tions was generally similar for 14C acetate, 14Cpalmitate, 14C oleate, and 14C linoleate in thecase of mycelium and fruiting body. Appar-ently, linoleic acid was utilized as source ofacetate for lipid biosynthesis in the fruitingbody. A significantly higher incorporation oflabel was seen in fruiting body sterol. Malatedehydrogenease activity increased in the myce-lium grown in the presence of lipids. Lipase ofPleurotus sajor-caju was inductive. The growthof Pleurotus sajor-caju was enhanced by in-creased lipid utilization. The implications ofthese results on commercial cultivation of thismushroom are discussed (Nair et al., 1990).

E. Vitamins

Mushrooms are a good source of severalvitamins (Zakia Bano and Rajarathnam, 1986).Species of Pleurotus are estimated to containpredominantly vitamins of B-complex and folicacid. Relative to Auricularia, Lentinus andVolvariella, the contents of thiamine, niacinand riboflavin of Pleurotus species were higher(Table 15). Considering the amount of vita-mins contributed by 100 g fresh Pleurotusmushrooms as % of the requirements level in-

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TABLE 15Vitamins a of Basidiopmycetes (mg per 100 g dry weight)

Ascorbic PantothenicSpecies acid Thiamine Niacin Riboflavin acid Folic acid b

Pleurotus 144 ± 22 1.46 ± 0.21 73.3 ± 3.35 7.10 ± 1.32 33.3 ± 2.00 1222 ± 101flabellatus

Pleurotus 92 ± 14 2.23 ± 0.33 66.6 ± 5.23 8.97 ± 1.11 24.3 ± 2.95 1346 ± 120eous

Pleurotus 111 ± 16 1.75 ± 0.23 60.0 ± 4.72 6.66 ± 1.22 21.1 ± 3.11 1278 ± 130sajor-caju

Pleurotus 113 ± 15 1.36 ± 0.15 72.9 ± 5.33 7.88 ± 1.00 29.4 ± 2.93 1412 ± 150florida

Agaricus 82 1.14 56.19 4.95 22.8 933bisporus

Auricularia n.a 0.16 4.10 0.48 n.a n.aLentinus n.a 0.40 11.90 0.90 n.a n.aVolvariella n.a 0.32 59.5 2.73 n.a n.a

Note: n.a = Not available.

a Mean of three sample determinations ± standard deviation.b µg 100 g dry mushrooms.


dicated by FAO/WHO (FAO, 1972) per personper day and allowing for differences in mois-ture contents, Pleurotus mushrooms are par-ticularly good sources for meeting the humanrequirements for riboflavin and folic acid(Table 16).

Considering the ease with which thePleurotus species can be grown on natural plant

wastes, their production and consumption wouldbe an efficient method of providing the vita-mins in the diet in the form of edible fruitingbodies. Solar radiation of Lentinus was shownto increase the D2 content severalfold, relatedto the duration of exposure (Takeuchi et al.,1990). Similar effect was also reported withHiratake and Enokitake (Kiribuchi, 1990). The

TABLE 16Vitamins Contributed by 100 g Fresh Pleurotus Mushrooms asPercent of the Daily Requirement Recommended by FAO/WHO a PerPerson

Ascorbic acid Thiamine Niacin Riboflavin Folic acid

Adult man 24–43 10–15 26–33 33–39 53–60(30) (1.2) (19.8) (1.8) (0.2)

Adult woman 24–43 13–19 36–46 46–54 53–60(30) (0.9) (14.5) (1.3) (0.2)

Note: Figures in parentheses are values in mg recommended intake by FAO/WHOper person per day.

a Report of a joint FAO/WHO Expert Group, FAO, Rome (1974).


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mycelium of Pleurotus ostreatus in liquid cul-ture was demonstrated to biosynthesize thia-mine, riboflavin, niacin, pyridoxin and biotinbut it failed to biosynthesize cyanocobalamin(Solomko and Eliseeva, 1988). Enzymic andnonenzymic thiamine decomposing factors inFlammulina velutipes are reviewed with 28references (Iijima, 1986). Methods to estimateD2 (ergocalciferol and preergocalciferol) andvitamin A, in dried Lentinus edodes, Enokitake,Hiratake, Nameko, Maitake, and Tsukuritake(Takamura et al., 1991; Yokokawa andTakahashi, 1990; Xu, 1989; Shah et al., 1989;Kobayashi et al., 1988) are described.

Mushrooms are known for their vitaminsof B-complex (Niacin, Thiamine, and B12),and folic acid (Rajarathnam et al., 1992). Theirability to contain these vitamins, even duringtheir growth on lignocellulosic wastes, eventu-ally substantiate their biosynthetic capacities.In fact, folate synthetase and B12-synthetaseenzyme systems (Iwai et al., 1977) have beendemonstrated in mushroom cells. Myceliumgrown in a synthetic medium to contain thesevitamins further supports their abilities tobiosynthesize the vitamins.

F. Flavor Components

In general, the mushroom flavor substancesare derivatives of fatty acids and nucleotides.Flavor is the most important inducement forpast and present widespread consumption ofwild and commercially grown edible mush-rooms. Maga (1976) has reviewed the subjectof volatile fractions of mushroom flavor. Asmany as 150 volatile compounds have beenidentified in various mushroom species(Pyysalo, 1976). A series of eight carbon (C8)compounds are believed to be the most impor-tant volatile flavor compounds. It has beendemonstrated that some of the C8 and C10compounds can be enzymatically formed fromlinoleic and linolenic acids, both of which areusually predominant in fruiting bodies (Tresslet al., 1982). The gills were found to be the

major compartment for the metabolic inter-conversion of fatty acids into aromatic com-pounds. In Lepista nuda, 1-octen-3-ol was themajor aroma trapped and linoleic acid was themajor fatty acid extracted, from whatever themorphhological tissue considered (Catherineet al., 1996). There was a preponderance of1-octen-3-ol in fresh fruiting bodies ofCantharellus cibarius, Coprinus atramentarius,and Leucocoprinus elaeidis. 1-octen-3-one hadthe highest aroma value in fresh fruiting bodiesof Psalliota bispora. Pyysalo (1976) has de-scribed the threshold values of flavors and theircharacteristics.

Of the several classes of flavor componentsidentified in the volatile extracts of Agrocybeaegerita, 1-octen-3-ol was found to be the maincomponent (Takama et al., 1978). Aroma stud-ies of Marasmius oreades with five differentextraction methods indicated 150 constituentsfor the dried mushroom and 13 for the freshmushrooms. The 1-octen-3-ol level on the driedproduct was 15% of that in fresh mushrooms.Comparison of the extraction methods (liquid-solid extraction, extractive distillation, steamdistillation, super critical CO2 extraction andhead space trapping) revealed large qualitativeand quantitative differences (Vidal et al., 1986).A paper electrophoresis followed by spectrom-etry at 260 nm is described for determination ofnucleotides (5-guanyllic acid and 51-inosinicacid) in mushroom soy sauce (Gu, 1989). Thevolatile components of raw and boiled Agari-cus bisporus by GC and MS are described (Ahnet al., 1987a,b). GMP was produced by Lentinusedodes during fermentation performed at 24 to27°C, pH 5 for about 6 h (Shangguan, 1988).

Ethyl linoleate, hexadecanoic acid, 9,12-octadecadienoic acid, β-sitosterol, and benzoicacid were identified for the first time from theChinese mushroom, Hobenbuehelia serotina(Cao et al., 1996). The main components of thefruit bodies of 10 frozen mushrooms were1-octen-3-ol, benzaldehyde, phenylethanol,(E-E)-2,4-decadienal and (E-Z)-2,4-decadienal.Lysidine, delta-cadinene, cis-sabinene hydrateand trans-sabinene hydrate were identified for

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the first time in mushrooms (Rapior et al.,1996a). Twenty-five volatile compounds wereidentified from the dichloromethane extracts ofthe fruiting bodies of Piptoporus betulins,Oligoporus caesius, Amanita rubescens,Paxillus involutus, Suillus grevillei, Suillusluteus, and Xerocomus subtomentosus (collectedfrom France). The main constituents were1-oceten-3-ol (14 to 75%; present in 5 species),3-octanol (1 to 40%; present in 3 species), (E)-2-decenal (12 to 40%; present in two species)and (E)-2-heptenal (20 to 30%; present in twospecies). Geranyl acetone and 1,8-cineole (eu-calyptol) were identified for the first time infungi (Rapior et al., 1996b). The white truffle(collected in central Italy) showed the impor-tant contribution of 2,4-dithiapentane to thearoma. At room temperature, the conversion of2,4-dithiapentane into dimethyl disulfide was amore important factor influencing flavor(Bellesia et al., 1996).

Benzaldehyde, benzyl alcohol, and 4-hydroxybenzaldehyde were the major flavorcompounds reported from fresh mushrooms ofAgaricus augustus, which were collected, fro-zen, and analyzed by GC-MS (Wood et al.,1990). Fischer and Grosch (1987) have experi-mented on the relative importance of mush-room flavors in Psalliota bispora. 1-octen-3-one, a minor component of the volatiles, showedthe highest aroma values in all samples. 1-octen-3-ol was the major compound in the extractsobtained from the fresh mushroom homoge-nate. Its aroma value in the extraction ap-proached that of the ketones, when the volatileswere isolated by vacuum distillation. Because1-octen-3-one was also found to be the mostsignificant odor compound in the cubed mush-room samples, it is concluded that this sub-stance, and not the alcohol is the most impor-tant volatile flavor compound in freshmushrooms. Several flavor compounds ofmushroom species are given in Table 17.

The ability of cells of Polyporus species toform several of the fragrances viz., linalool,geraniol, citronellol, α-terpineol, β-phenylethylalcohol, and benzyl alcohol is evidenced. Short

incubation time favored the formation of terpe-nes and longer incubation favored aromaticcompounds (Llerena et al., 1987). The neutralvolatile constituents produced by shake flaskcultured mycelium of Polyporus durus com-prised aliphatic and aromatic alcohols, lactonesand various carbonyl compounds, and ses-quiterpenoids. The occurrence of five 2,3-un-saturated 4-olides compounds (gammalactones),some of which were identified for the first timein nature, is characteristic of the fungus. Thepresence of a synthetic triglyceride in the nutri-ent medium strongly favored the formation oflactones and other volatile flavor compounds(Berger et al., 1986).

Mushrooms collected from three majorcultivation regions in Taiwan were divided intobutton, and open mushrooms, separated intocap and stipe. Among the 51-nucleotides,51-CMP, and 51-AMP were present at greaterlevels than 51-UMP and 51-XMP. Expressedsynergistic effect of Glu and 51-GMP for mono-sodium glutamate, was higher in the cap thanstipe. It decreased when the cap opened (Tsaiand Tsai, 1987). 51-GMP derived from endog-enous RNA was high in Shiitake (44%), among13 kinds of vegetables studied. The maximumamount of 51-GMP that can obtained was at thepeak of nuclease activity curves, which corre-spond to temperatures of 65 to 75°C (Nguyenet al., 1988).

Supplementation of the rice straw substratewith cotton seed powder caused a difference inthe relative concentrations of the flavor con-stituents of Pleurotus flabelatus fruiting bod-ies. The major constituents were 2-pentanone,3-pentanone, methyl butyrate and 2-methyl-3-pentanone (Rajarathnam et al., 1990). Supple-mentation of the growth substrate with saf-flower oil at casing, did not affect 1-octen-3-olcontent of Agaricus bisporus mushrooms. The1-octen-3-ol content was observed to decreaseduring their post-harvest storage (Mau et al.,1991).

Enzymic formation of 1-octen-3-ol in thecultivated mushroom was studied. The optimalactivity of lipoxygenase and hydroperoxide

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TA

BLE

17

Fla

vor

Com

pone

nts

of M

ushr

oom

Spe

cies

Mus

hroo

msp

ecie

sM

etho

dC

ompo

nent

sR

ef.

Lent

inus

Are

C8

alco

hols

and

S c

ompo

unds

; l-o

cten

-3-o

lC

hen

et a

l. (1

986b

)ed

odes

and

2-oc

ten-

1-ol

, th

e m

ajor

C8

com

poun

ds;

Lent

hion

ine,

ete

rath

iane

, an

d tr

ithio

lane

are

the

cycl

ic S

-com

poun

ds;

the

form

er f

orm

eden

zym

atic

ally

fro

m li

nole

nic

acid

and

the

latte

r fr

om e

nzym

atic

rea

ctio

ns o

f le

ntin

ic a

cid

as s

ubst

rate

and

non

-enz

ymat

ic p

;ym

eriz

atio

n of

met

hyl d

isul

fide

Lent

inus

GC

-MS

Fre

sh1-

octe

n-3-

ol (

71.0

5%),

eth

yl a

ceta

te (

1.17

%),

edod

es2-

octe

n (1

.22%

), a

nd o

ctyl

alc

ohol

(1.

05%

)B

oile

d1-

octe

n-3-

ol (

83.6

8%),

eth

yl a

ceta

te (

2.24

%),

Ahn

et

al.

(198

7a)

2-oc

teno

l (1.

55%

), o

ctyl

alc

ohol

(1.

28%

), a

nd1,

2,4-

trith

iola

ne (

1.91

%)

(sul

fur

cont

aini

ng)

Ple

urot

usG

C a

nd G

C-M

SF

resh

3-oc

tano

l (46

.01%

), 3

-oct

anon

e (1

8.75

%),

ostr

eatu

s1-

octe

n-3-

ol (

15.3

9%),

isob

utyl

alc

ohol

(3.4

8%)

and

isoa

myl

alc

ohol

(3.

07%

)≡

89.0

4% o

f th

e to

tal a

rom

aC

ooke

d1-

opct

en-3

-ol (

66.5

0%),

3-o

ctan

ol (

10.9

9%),

Ahn

and

Lee

(19

86a)

3-oc

tano

ne (

9.77

%),

1-o

cten

-3-o

ne (

1.23

%),

octy

l-alc

ohol

(1.

12%

), a

nd o

ctin

ol (

0.96

%)

≡ 89

.61%

of

the

tota

l aro

ma

Lent

inus

51 -C

MP

, 51 -

GM

P,

and

51 -A

MP

cou

ld b

eS

ekiz

awa

et a

l. (1

988)

edod

esco

mpl

etel

y se

para

ted

on a

rev

erse

d co

lum

n;C

anth

arel

lus

L. e

dode

s an

d G

. fr

ondo

sa w

ere

rela

tivel

yci

bariu

sric

h in

51 -

nucl

eotid

es;

P.

oste

reat

us c

onta

ined

Sar

codo

nhi

gher

CM

P c

onte

ntas

prat

usB

olet

otop

sis

leuc

omel

asG

rifol

afr

ondo

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tical

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TA

BLE

17

(con

tinue

d)F

lavo

r C

ompo

nent

s of

Mus

hroo

m S

peci

es

Mus

hroo

msp

ecie

sM

etho

dC

ompo

nent

sR

ef.

Ple

urot

usG

C-M

S1-

octe

n-3-

ol,

3-oc

tano

ne,

3-oc

tano

l,1,5

-Ju

ng a

nd H

ong

ostr

eatu

soc

tadi

en,

3-on

e, n

-hex

anol

, ph

enol

,(1

991)

(str

ains

)n-

pent

anal

, n-

hexa

nol,

n-pe

ntan

olP

leur

otus

florid

a

Tric

holo

ma

GC

and

GC

-MS

Raw

1-oc

ten-

3-ol

(73

.95%

), m

ethy

l cin

nam

ate

Ahn

and

Lee

mat

suta

ke(1

2.52

%)

2-oc

teno

l (7.

62%

), a

nd o

ctyl

(198

6b)

alco

hol (

2.78

%)

≡ 96

.87%

of

the

tota

lar

oma

Coo

ked

1-oc

ten-

3-ol

(64

.94%

), m

ethy

l cin

nam

ate

(22.

03%

), 2

-oct

anol

(7.

68%

) an

d oc

tyl

alco

hol (

3.21

%)

≡ 89

.61%

of

the

tota

l aro

ma

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lyase for 1-octen-3-ol formation was at pH 5.0to 7.0. The highest amount of 1-octen-3-ol wasproduced at pH 6.0. During the crop cycle, the1-octen-3-ol content of mushrooms varied from,19.3 to 37.2 ppm. More 1-octen-3-ol was pro-duced in the gills than other morphologicaltissues. During post-harvest storage at 12°C,enzyme activity and 1-octen-3-ol content de-creased dramatically over time (Mau et al.,1992).

Procedures are described for the produc-tion and manufacture of mushroom flavorsconsisting of several compounds (Hasegawa,1986) from culture extracts (Komai et al., 1986).In submerged culture, typical flavor compoundssynthesized by mushrooms include volatilesderived from the metabolism of fatty acids,especially the mushroom alcohol, 1-octen-3-ol; biotechnological improvements are how-ever required to achieve flavor levels satisfac-tory for commercial applications. (Hadar andDosoretz, 1991). Abraham and Berger (1994)have detailed the flavor impression notes fromliquid cultures of 20 mushroom species(Table 18).

G. Nucleic Acids

Nucleic acid content of mushroom is gen-erally only a few percent (~3%), which is lowcompared with that of bacteria, yeasts, and al-gae (10 to 20%) (Kurkela et al., 1980; ZakiaBano and Rajarathnam, 1988). Ribonucleic acid(RNA) was found to be the predominant nucleicacid in all four species of Pleurotus studied(Khanna and Garcha, 1986). Compared withthe nucleic acid content of algae (Viikari andLinko, 1977), yeast and other microbes, thenucleic acid content of Pleurotus is quite low.The Protein Caloric Advisory Group of theUnited Nation System (FAO/WHO, 1970) haspublished recommendations for the maximumacceptable nucleic acid content. According tothese recommendations, a daily intake of 4 g ofnucleic acid, 2 g of which are obtained fromsingle cell protein represents a safe practical

limit for most of the adult population. On thebasis of the PAG recommendations, consump-tion of as much as 200 to 250 g fresh Pleurotusper person per day, should not prove hazard-ous. Thus, Pleurotus as a class of single cellproteins, does not pose the problem of nucleicacid content in human nutrition, unlike someother microbes.

In Flammulina velutipes, the nucleic acidcontent varied from 5.5% (mycelia) to 3% (fruit-ing body) of the dry weight. The proportion ofDNA was small, not over 0.05% of the dryweight.

In addition to nucleic acids, many nucle-otides occur in mushroom species. Quantita-tive changes of these nucleotides in mushrooms,due to the various pretreatments are delineated(Table 19) (Sekizawa et al., 1992).

Thus, despite their fast growth, particularlyin the phase of fructification, nucleic acid con-tents of mushrooms are quite safe from thepoint of human consumption. The operation ofvarious nucleases and presence of bases in themushroom cells required for their formation,elucidate their ability to form the nucleic acids.In view of DNA serving as the heritable mate-rial and RNA working for protein biosynthesis,coupled with the fact of fast rate of cell multi-plication during fructification, this emphaticallypronounces the “active nucleic acid metabo-lism”. Any objective to ultimately transform/regulate, the features/properties of mushroomslies in transforming these nucleic materials andthus, the significance of role of molecular biol-ogy herein.

H. Minerals

About 10% of the ash content of dry fruit-ing bodies represent the minerals. Potassium,calcium and ferrous iron constitute the majorminerals of mushrooms (Table 20). Trace ele-ments like Cu, Bo, and Co are also present.However, mushrooms are reported to have theproperty of bioaccumulating minerals from thegrowth substrates and this should warn the

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TABLE 18Odor Assessments of Classified Flavor Volatiles from 20 Strains of Mushroom Grown inLiquid Culture

Compoundalcohols Odor assessment Compound Odor assessment

1-butanol Amyl alcohol like 2-methyl-3-hexanol Pungent1-pentanol Fusel oil 2-heptanol Pungent, herbaceous1-hexanol1-heptanol1-octanol2-propanol2-methyl-1-propanol

2-butanol2-buten-1-ol2,3-butanediol Fatty2-methyl-1-butanol Pungent3-methyl-1-butanol

3-methyl-2-buten-l-ol Pungent2-pentanol2-methyl-3-pentanol Pungent2-methyl-2-pentanol Pungent3-methyl-1-pentanol Wine-like, pungent4-methyl-pentanol3-hexanol2(E)-hexen-1-ol3-methyl-1-hexanol Pungent 3-hydroxy-3-methyl-butanone4-methyl-3-penten Green Methyl 3-methyl butanoate Fruity2-one Methyl benzoate Fruity3-hexanone Methyl 4-methoxybenzoate Floral, hyacinth2-heptanone Banana Methyl 2-methoxybenzoate Sweet, floral3-octanone Fruity, lavender Methyl 4-hydroxybenzoate1-octen-3-one Mushroom Methyl phenylacetate Honey3-octen-2-one Methyl 4-methoxyphenyl-1-phenylethanone Meal Acetate Sweet4-hydroxy-4-methyl Methyl 2,4-dihydroxy 3,6-2-pentanone Dimethylbenzoate OakmossAldehydes Methyl 2,4-dihydroxy-6- Sweet, mossy

MethylbenzoateHexanol Fatty, green Methyl 2-hydroxy-4-methoxy Earthy, mossy

6-methylbenzoateHepta-nal Oily, fatty2-methylpentanol Fruity Methyl 2,4-dimenthoxybenzoate Sweet, phenolic2-methyl-2-butenal Green Methyl 3,6-dichloro-2-methyl- Sweet

BenzoateBenzaldehyde Bitter almond Methyl 2-furancarboxylate MushroomPhenylacetaldehyde Harsh, hawthorn Methyl 3-furancarboxylate Mushroom2-furancarboxaldehyde Sweet Methyl 3-pyridinecarboxylate3-phenyl-2-propenal Pungent, spicy Methyl 2-pyridinecarboxylate4-methoxybenzaldehyde Anise Lacontes2,4-dihydroxy-3,6- Sweet, phenolic 4-butanolide Faint, butterDi-methylbenzaldehyde2-hydroxy-4-methoxy- 4-pentanolide6-methylbenzaldehyde Sweet 2-hydroxy-3,3-dimethyl-4-butanolideesters

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TABLE 18 (continued)Odor Assessments of Classified Flavor Volatiles from 20 Strains of MushroomGrown in Liquid Culture

Compoundalcohols Odor assessment Compound Odor assessment

Methyl butanoate Ethereal 4-hexanolideEthyl hexanoate Fruity, apple 4-heptanolide Coconut, sweetmethyl 3-hydroxy

Butanoate Fruity

Compound Odor assesment

2-hepten-4-olide4-octanolide Coconut, fatty2-octen-4-olide Fruity4-nonanoline Fatty, coconut4-decanolide Peach4-methyl-5-hexanolide Fruity5-hexanolide

Phenols

Phenol Phenol4-methylphenol Smoky, phenolic3-methoxy-5-methyl-phenol Woody, tary3-methoxy-2,5-dimethyl-phenol Oakmoss3-hydroxy-5-methylphenol Sweet, smoky4,5-dimethoxy-2-methylphenol Sweet phenolic2-methoxyphenol Sweet, phenolic4-methoxyphenol Sweet3,5-dimethoxyphenol Smoky2,3-dimethylphenol Smoky5-methoxy-2,3-dimenthylphenol Sweet2-methyl-4(2-propenyl) Clove-likephenol

Adapted from Abraham and Berger, 1994.

consumer that the naturally grown mushroomshould be regularly monitored for mineral con-sumption, to be safe from untowardly incidents(Woggon and Bickerich, 1978; Tyler, 1980;Enke et al., 1977, 1979).

In an analysis of minerals in Agaricusbisporus, Pleurotus sajor-caju and Volvariellavolvacea, the cap had a higher content of min-erals than stipe. Agaricus bisporus showed high-est contents of P, Ca, Mg, K, Cu, and Mn;Pleurotus sajor-caju S, Na, and Zn; andVolvariella Fe (Verma et al., 1987). The caps,of Agaricus bisporus and Pleurotus ostreatus,

also had greater concentrations of mineral ele-ments than stipes. The former had higher P, K,and Ca, but lower trace element concentrationsthan the latter, which was higher in Mg, B, Cd,Fe, and Mn concentrations (Vetter, 1994a,b).The average distribution of minerals inPleurotus sajor-caju, Agaricus bisporus andLentinus edodes showed that except Sb, allother minerals preferred residence in the pileus(Latiff et al., 1996). Mineral contents werehigher in caps than stipes in Lentinus edodes(Vetter, 1995). All the three mushrooms,Lentinus subnudus, Psathyrella atroumbonata

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TABLE 1951-Nucleotide Contents (mg per 100 g Dry Weight) in Mushroom Species

Treatment 5 1-Nucleotidesfor mushroomstorage and

extraction con- 5 1- 51- 51- 51- 51- 51-Species ditions a CMP UMP AMP GMP IMP XMP Total

1 2 3 4 5 6 7 8 9

Armillariella A — 32 33 147 3 — 215mellea B — 44 62 140 5 — 251

C — 14 7 70 10 9 110D — 38 36 166 240E — 37 31 254 322F — 21 14 86 3 5 129G — — — — — — 0H — — — — — — 0

Grifola A — 77 129 232 — — 438frondosa B — 84 91 212 — — 387

C 81 57 65 199 — — 402D — 51 77 141 5 — 274E — 47 72 167 6 — 292F 108 50 102 108 — — 368G — 2 — — — — 2H — — — — — — 0

Hygrophorus A — 15 10 7 — — 32russula B — 12 6 11 — — 29

C 57 12 — 22 39 — 130D — 2 13 2 — — 17E — 2 — 2 — — 4F 43 — 5 3 2 — 53G 3 2 — — — — 5H — — — — — — 0

Lactarius A 198 136 217 262 — — 813hatsudake B 198 249 120 154 — — 717

C 73 101 — 32 — — 206D 228 465 374 396 38 — 1,501E 242 286 203 251 27 — 1,009F — 137 — — — — 137G — 3 6 6 — — 15H — — 21 5 — — 26

Lentinus A 151 40 51 209 — — 387edodes B 161 58 59 123 — — 401

C 144 67 50 79 — — 340D — 49 54 102 — — 205E — 97 97 144 — — 338F — 62 55 79 — — 196G 39 5 — — — — 44H 23 10 6 9 — — 48

Lyophyllum A — 137 91 145 — — 437fumosum B — 204 76 191 — — 471

C — 115 — 78 — — 193D — 127 133 184 — — 444E — 161 155 196 — — 512F — 107 — 39 — — 146G — 2 — — — — 2H — — — — — — 0

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TABLE 19 (continued)51-Nucleotide Contents (mg per 100 g Dry Weight) in Mushroom Species

Treatment 5 1-Nucleotidesfor mushroomstorage and

extraction con- 5 1- 51- 51- 51- 51- 51-Species ditions a CMP UMP AMP GMP IMP XMP Total

1 2 3 4 5 6 7 8 9

Ramaria A — — 2 22 — — 24botrytis B — — 14 54 — — 68

C — — — 7 — — 7D — — 6 40 — — 46E — 3 13 50 — — 66F — — — 18 — — 18G — 2 — — — — 2H — 6 11 11 — — 28

a Drying at 0°C reduced atmosphere : A, boiling for 10 min; B, boiling for 30 min; C, after soakingin water for 3 h at 20°C, boiling for 30 min. Drying by heated air: D, boiling for 10 min; E, boilingfor 30 min; F, after soaking in water for 3h at 20°C, boiling for 30 min.Salting: G, after desalting (by soaking in hot water for 10 min, then soaking in water 5 h at roomtemperature), boiling for 30 min; H, after desalting (by soaking in water for 24 h at roomtemperature), boiling for 30 min.

Adapted from Sekizawa et al., 1992.

TABLE 20Mineral Content in Mushroom Species a

Species Ca P K Fe Cd Zn Cu Pb

mg per 100 g ppm

Pleurotus eous 23 1410 4570 90 0.4 82.7 17.8 1.5Pleurotus florida 24 1850 4660 184 0.5 111.4 15.8 1.5Pleurotus 24 1550 3760 124 0.5 58.6 21.9 1.4flabellatus

Pleurotus 20 760 3260 124 0.3 129.0 12.2 3.2sajor-caju

Pleurotus 33 1348 3793 15.2 nd nd nd ndostreatus

Agaricus 23 1429 4762 186 nd nd 12.8 ndcampestris

Volvariel 58 1042 3333 177 nd nd nd nddiplasia

Lentinus 118 650 1246 30.3 nd nd nd ndedodes

a On dry weight basis.


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and Termitomyces striatus were good sourcesof Mg, Zn, and Fe (Alofe et al., 1996). Radio-active cesium is reported from Lentinus edodesmushroom grown on Japanese Oak in Hokkaido(Okui and Kobayashi, 1990). The contents ofCu, Zn, Mn and Hg in the mushrooms grownon wood were lower than mushrooms grown inthe soil (Kawai et al., 1990). An improvedmethod for assay of germanium is described.The higher content of germanium in Ganodermalucidium like in ginseng is reported (Chiangand Wann, 1986). The interference of Si inmineral estimation of mushrooms is discussed(Hedrich, 1988). The arsenic contents of 80species of mushrooms were determined. Someof the wild species of Agaricus, such as Agari-cus macrosporus, even exceeded 10 mg kg–1

and Laccaria amethystina contained on aver-age 82 mg kg–1 (Stijve and Bourqui, 1991).Mineral composition of Pleurotus ostreatus isalso dealt with, and lead and mercury levels didnot exceed the permissible limits (5 and0.5 mg kg–1 dry, respectively, for lead and mer-cury). Arsenic content in all samples was be-low 0.01 mg kg–1, maximum permissible quotedat 5 mg kg–1 dry (Strmiskova et al., 1992).During cultivation of Pleurotus sajor-caju onwaste products (Ricinus communis and Morusalba), the mineral contents in different spentresidues were found to be less than in the rawsubstrates, as these were utilized by the grow-ing mycelium; K and P contents predominatedin the mushroom (Madan et al., 1992).

Bioaccumulation of minerals in Agaricusand Pleurotus was observed (Bressa et al., 1988,Vetter, 1989). Uptake and accumulation of Hgand Au were studied in Agaricus bisporus byraising mushrooms on compost incorporatedwith radioactive tracers (Byrne and Tusek-Znidaric, 1990). In Pleurotus ostreatus, fruit-ing body production was unaffected up to Cdlevels of 285 mg kg–1 dry substrate (Faveroet al., 1990). The accumulation of Cd, Zn, Pb,Cu, Ni, and Mn in the fruiting bodies of 34mushroom species analyzed was associated withthe intensity of environmental pollution andthe distance from the source of pollution

(Hedorov and Parfenova, 1990). Actinoid-serieselements were selectively sorbed from indus-trial waste waters by mushrooms. Inonotusmikadol was used to selectively recover U froman aqueous solution containing 10 ppm U at91.5% yield (Sakaguchi et al., 1990). Therewas an uptake of heavy metals by Azolla pinnataand their subsequent translocation into the fruit-ing bodies of the edible mushroom Pleurotussajor-caju, when grown on such metal-enrichedsubstrate. A high concentration of heavy met-als in the enriched substrate reduced the bio-logical efficiency of mushroom production. Theuptake of heavy metals in the substrate as wellas their translocation into the fruiting bodiesincreased with an increasing concentration ofthese metals in the exposed solution and thesubstrate (Jain et al., 1989). There was an ab-sorption of Pb, Cd, Zn, Mn, Co, Cu, Ni, and Feby duck weed, Lemna minor, and their translo-cation into the fruiting bodies of the ediblemushroom Pleurotus sajor-caju, grown onmetal-enriched duck weed. A high concentra-tion of heavy metals in the substrate reducedthe biological efficiency of mushroom produc-tion (Jain et al., 1988).

Psalliota hortensis showed maximum Secontent (29.65 ng g–1) compared with severalfruits and vegetables, determined by hydridegeneration (Diaz-Alarcon et al., 1994). InPleurotus sajor-caju, substrate with Pb reducedbiological efficiency of fruiting body produc-tion, while Hg caused maximum reduction ofprotein in fruiting bodies (Purkayastha et al.,1994).

The study of Ag uptake by Agaricusbisporus from an artificially enriched substrateshowed the inverse correlation of the biocon-version factor in the mushroom with Ag in thesubstrate (Falandyszm et al., 1994). Use ofAgaricus campestris as a bioindicator speciesto trace the concentrations of Ag was limited insoil polluted with other heavy metals like Pband Cd (Falandyszm and Danisiewicz, 1994).Phanerochaete chrysosporium was most effec-tive in sorption of Pb compared with Polyporusostreiformis, Volvariella volvacea, and

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Pleurotus sajor-caju (Dey et al., 1995). For thefirst time, Coprinus species were shown able tomethylate mercury after the transformation ofHg from the soil humus (Fischer et al., 1995).

Content of toxic metals was greater forwild than cultivated mushrooms (Procida andPertoldi, 1995). In mushrooms grown wild nearthe viscinity of a mercury smelter, particularlyin Lepista procera concentrations of mercurywere extremely high (119 to 2100 mg kg–1 drymatter). In Lepista procera and Lepista nudanear the copper smelter area Cu concentrationsexceeded 200 mg kg–1, and there were alsohigh lead values 26.4 and 15.3 mg kg–1 drymatter, respectively. Thus, the mushrooms fromboth areas should not be consumed (Kalac et al.,1996). Mushrooms showed accumulation ofcesium and radiocesium from forest litter(Zagrodzski et al., 1994). The results of study-ing the distribution of Na, K, Pb, Cs, and 137Csin some Austrian mushroom species showed ahigh correlation coefficient (0.80) between thecontents of 137Cs and Na, but none between137Cs and K (Ismail, 1994). The activity of Cs-134 and Cs-137 was measured in mushroomsfrom Poland (Grabowski et al., 1994). The high-est measured 137Cs activity 157 KBQ/kg–1 drymass was recorded in Xerocomus badius(Mietelski et al., 1994). Uptake of radiocesiumby different mushroom species in Germany andJapan are reported (Kammerer et al., 1994,Yoshida et al., 1994, Sigiyama et al., 1994).The concentration of 137Cs in mushrooms iscontrolled by their species, environmental andweather conditions; and by dynamics of radio-nuclides dissolution. The contribution of mush-rooms in 137Cs biogeochemistry exceeds that ofhigher plants (Tsvetnova and Scheglov, 1996).

Mushrooms derive their minerals from thegrowth substrate and artificial culturing on pre-pared substrates cannot be harmful. However,their property of bioaccumulation warns theconsumers that mineral analysis of mushroomspicked from the natural growth, should be ex-amined for possible mineral contamination(s).Other than this, cultivated mushrooms serve asgood source of most of the required minerals in

essential concentrations, with safe limits forconsumption up to 100 g (fresh) day–1 (ZakiaBano et al., 1981).

I. Pigments

Some of the mushroom species are pig-mented. Pleurotus eous is one such mushroom(Rajarathnam and Zakia Bano, 1987), withpleasant pink coloration, the intensity of whichfades in presence of light and high temperature.The field of research on chemical and biologi-cal function of mushroom pigments remainsmostly unexplored. Takekuma et al. (1994) haveundertaken the first investigation on the isola-tion and characterization of a pink pigment inthe edible mushroom, Pleurotus salmoneo-stramineus. The beautiful pink color of themushroom turns whitish in color after its fullgrowth. The pigment was isolated from themushroom (during its growth phase), and thechromoprotein was purified by repeated gelfiltration (on Sephadex G-50) of the water ex-tract of the well-ground mushroom. The pinkpigment (indolone) is a glycoprotein with agalactose chain and three metals (Zn, Fe, andCu). It is concluded that the indolone plays avery vital role in the photochemical generationof oxygen from water, suggesting the involve-ment of the indolone in a photosynthesis likephenomenon.

Three orange pigments, austocystene-f,averufin, and averufanin (previously knownfungal metabolites), were isolated fromArmillaria mellea (Ayer and Macaulay, 1987).Atromentin (pigment) occurs in fruiting bodiesof Paxillus atrotomensosus, mainly in the formof the colorless leucomentins (Holzapfel et al.,1989).

J. Chitin

Chitin, the homopolymer of N-acetyl-D-glu-cosamine is a prominent and a characteristiccomponent of the mushroom cell wall. This

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component is invariably not noticed in thegrowth substrate; however, it is very muchpresent in the mushroom cell walls, eventuallyreflecting on its synthesizing ability by themushroom species. Chitin content varies from4 to 9% on a dry weight basis depending on thespecies/strain. A significant quantity of mush-room nitrogen is thus lodged in chitin. Theerror introduced here, is possibly excluded bythe use of a factor 4.38 instead of 6.25 forconversion of N into protein (Crisan and Sands,1978). This factor has been adopted for mush-rooms in several food composition tables (FAO,1970; FAO and WHO, 1972; Leung et al.,1972). This subject is discussed by Kurkelaet al. (1980). The Aphyllophorales species,which are xilophagus wood-rotting fungi, havea lower chitin content (Vetter and Siller, 1991).Species of Boletales, Agaricales, and Russulaleshave significantly higher (8 to 9% of dry mass)chitin in the fruiting bodies (Table 21). Thedifference in chitin content of systematicallydifferent fungal groups is explained by differ-ent types of nutrition such as wood-rotting,saprophytic, and mycorrhizal. The wood-rot-ting species have a significantly lower content,while the others have a higher chitin content.Invariably the caps contain more chitin thanthe stipe. The chitin content of 15 species offield grown edible mushrooms was in the rangeof 1.87 to 6.93% of total dry mass (Ofenbeher-Miletic et al., 1984). The content of total ‘CrudeFiber’ (fungin) and the proportion of chitin andcellulose in it were determined in several mush-rooms (Table 22).

In fact, estimation of glucosamine in thegrowth substrate in solid state fermentation bymushroom species is an estimate of the extentof growth. Rajarathnam (1981) had observedan increase in the glucosamine content of therice straw substrate during the growth ofPleurotus flabelatus, until the end of the spawnrun; during cropping there was a decrease in itsconcentration, obviously indicating its utiliza-tion in the construction of the fruiting bodies.Hexosamine content was employed to estimatethe fungal biomass in solid substrate by

Matcham et al. (1985). The high hexosaminecontent in wooden logs colonized by Lentinusedodes was correlated with high subsequentmushroom yields and after repeated fruiting,the hexosamine content decreased. The muchgreater yield of mushrooms, particularly fromthe second and third fruiting cycles lends sup-port to the contention that the high hexosaminecontent is related to high subsequent yields ofmushrooms and that repeated fruiting decreasesthe hexosamine content (Tokimoto and Fukuda,1981).

A stable chitin synthetase preparation ofhigh specific activity was assayed from myce-lia of Coprinus cinereus (Pfefferle and Anke,1989). In Pleurotus ostreatus, both chitinaseand β-N-acetylglucosaminidase in the myceliaappeared to participate in hydrolysis of cellularchitin to form N-acetylglucosamine, whichmight be used as material for the formation offruiting bodies or an energy source (Iwamotoet al., 1990). Isolation, purification, and assayof chitinase and chitinbiase from puffballs weredescribed (Zikakis and Castle, 1988). 3,5-dichloro-4 methoxybenzyl alcohol, a novelnatural metabolite, was reported from the sub-merged cultures of a Stropharia species, due toits inhibitory activity toward chitin synthase(Pfefferle et al., 1990). Hexachlorophenestrongly inhibited solubilized chitin synthase;the inhibition could be reversed by the additionof lecithin. There was a necessity of the chlo-rine substituents, of the synthetic analogues,for the enzyme inhibition.

K. Polysaccharides

Polysaccharides (PS) denote a medicinallyvaluable group of mushroom carbohydrates.Their solubility coupled with their medicinalproperty to regress Sarcoma-180 tumors repre-sent the antitumor property of mushrooms.Chemically, they are mainly homo- or hetero-glucans with β-1 → 3 and 1→ 6 glucosidiclinkages. Substantial work is being done ontheir isolation, fractionation, purification, char-

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TABLE 21Chitin Content of Mushroom Species

Fungi sampleand Chitin contentlocality (% dry weight)

AphyllophoralesTrametes gibbosa 1.07Gandoerma lucidum 2.40Lactiporus sulphureus 2.49Cantharellus cibarius 2.72

AuricularialesHineola auricula-judae 1.92

PolyporalesPleurotus ostreatus“G — 32” Hut 3.31“G — 32” Stiel 2.42“H — 7” Hut 3.06“H — 7” Stiel 2.36“G — 24” Hut 2.93“G — 24” Stiel 2.16

BoletalesBoletus impolitus 6.00Boletus luridus 6.58Suillus granulatus 6.36Suillus granulatus 8.08Xerocomus subtomentosus 3.68

AgaricalesTricholomataceaeLepista nuda 7.40Lepista irina 5.70Lepista inversa 7.60Tricholoma terreum 2.77Melanoleuca melaleuca 7.87Marasmius oreades 6.56

AmanitaceaeAmanita phalloides 4.06Amanita verna 4.97Amanita rubescens 6.26

AgaricaceaeAgaricus abruptibulbus 2.93Agaricus purpurellus 9.68Macrolepiota procera 6.73Macrolepiota rhacodes 3.36

CoprinaceaePsathyrella candolleana 5.05

StrophariaceaeHypholoma fasciculare 2.70

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TABLE 22Fungin and Chitin Contents of Mushroom Species

Pure Fungin a

Fungin Chitin (%)

Species (% on dry Weight basis) Chitin Cellulose

Boletus edulis 8.39 4.71 56.10 43.90Coprinus comatus 7.81 4.07 52.06 47.94Coprinus disseminatus 8.35 4.00 44.66 55.34Coprinus atramentarius 6.77 2.34 34.51 65.49Russula cyanoxantha 13.62 6.93 50.89 49.11Lactarius deliciosus 7.36 2.84 38.57 61.43Lactarius piperatus 8.61 4.43 51.47 48.53Tricholoma rutilans 7.93 3.31 41.76 58.24Tricholoma colossus 9.17 5.11 44.62 55.38Tricholoma albobruneum 9.14 3.96 43.35 56.65Lyophyllum aggregatum 7.57 2.85 37.70 62.30Agaricus campestris 7.87 5.33 67.72 32.28Kuhneromyces mutabillis 7.96 3.55 44.66 55.34Lentinellus cochleatus 4.45 1.87 42.05 57.95Cantharellus cibarius 6.86 4.27 62.20 37.80

a Chitin and cellulose contents of pure fungin.

Adapted from Ivanka et al., 1984.

TABLE 21 (continued)Chitin Content of Mushroom Species

Fungi sampleand Chitin contentlocality (% dry weight)

RussulalesRussulaceaeRussula heterophylla 7.26Russula luteotacta 5.19Lactarius quietus 6.17Lactarius insulsus 5.77Lactarius piperatus 2.96Lactarius vellereus 6.70Lactarius chrysorrheus 4.32

Adapted from Vetter and Siller, 1991.

acterization and elucidation of biological prop-erties, in a number of species (Table 23).

Cultural conditions required for the pro-duction of extracellular polysaccharides fromGrifola fronodosa were optimized (Suzuki et al.,1987). Eleven mushroom strains were observedto produce exopolysaccharides (ep) from the

mycelium; ep of Auricularia auricularis showed61.2% total carbohydrates, representing rham-nose (Cavazzoni and Adami, 1992). Atomachin(1988) has described a procedure for the manu-facture of anti-tumor glucan PS from Coriolusversicolor. Neutral and acidic PS were formedin cultures of several mushroom species grown

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TABLE 23Polysaccharides from Mushroom Species

Species Properties/chemical nature Biological function Ref.

Agaricus Hot water extracted-neutral/ Increased the survival Mizuno et al.acidic rate of Sarcoma-180 mice (1989a; 1989b)

Agaricus blazei D-glucan protein complex Antitumor Kawagishi et al.(1990)

Agaricus blazei Water insoluble, β-D-glucan Antitumor Kawagishi et al.+ protein (1990d)

Agrocybe Alkali soluble D-glucan; Mol. Antitumor against Kino et al.cylindracea Wt. 5,60,000, β-D glucan Sarcoma-180; (1989)

Flammulina Inhibited growth of Zhao et al.velutipes Sarcoma-180; increased (1988)

life span of the miceby 29%

Flammulina PA5DE; glucose:mannose; inhibited the growth of Cao et al.velutipes fructose in 15.83: 1.7:1.0 ratio implanted Sarcoma-180 (1990)

with β1 → 3 and β1 → 6 solid tumor in miceglucosyl linkages

Gandoerma lucidumLentinus edodes Polysaccharide of extracts Anticomplementary Jeong et al.Cordyceps species activity (1990)Agaricus campestrisGandoerma lucidumGrifola frondosa Polysaccharides; β-D glucans Antitumor against Mizuno et al.Agaricus blazei Sarcoma-180 (1988)Grifola frondosa Hot water extractable, acid Antitumor Nishida et al.

insoluble and alkali soluble, (1988)contains 30% protein

Grifola frondosa Alkali soluble, β-D-glucan Kato et al.(1990)

Lentinus edodes Protective action against Lin and Haungexperimental liver injury (1987)

Lentinus edodes Theta composition of Zheng et al.Polystictus polysaccharide (1988)versicolor

Lentinus edodes Polysaccharide Stimulated immune function Cao et al.of mice (1989)

Pleurotus Heteroglycan, galactose, Mirjana et al.ostreatus mannose and fructose glyco- (1988)

sidic linkage α-D typePleurotus Polysaccharide Lowered cholesterol Bobek et al.ostreatus content in serum and liver (1991)

in syrian hamstersPolyporus Polysaccharide; β-1 → 3 and Antitumor activity Ito et al.confluens β-1 → 6 glucan (1991)

Polyporus Composed of mannose; galactose: Antitumor Zhu et al.umbellatus glucose in 20:4:1 (1988)

Polyporus Polysaccharide Prevention of liver Wang et al.versicolor cancer (1996)

Polystictus Polysaccharide Useful or prevention Xu et al.versicolor of lepatoma (1989)

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on Czapek-Dox liquid medium (Teaumroongand Picnyangkura, 1987). The PS from cul-tured mycelia of Pluteus cervinus, Hydnumrependum, Pleurotus pulmonarius, andLaccaria laccata had anti-tumor activities. ThePS of the first fungus was shown to be aheteroglucan (glucose 94.4% galactose 3.6%;mannose 2%) associated with a protein moietythat contained 17 amino acids (Chung and Kim,1985). Extracellular PS from the mycellium ofVolvariella volvacea exhibited hypocholester-olemic activity in rats with alimentary-inducedhypercholesterolemia (Geung, 1996). PS puri-fied from the mycelium of Phellinus linteusexhibited a wider range of immunostimulationand anti-tumor activity than other basidiomycetePS (Kim et al., 1996). D-mannan from the wa-ter extract of Dictyophora idusiata containedmannose (~96%) and traces of glucose andgalactose (Hara et al., 1988). The acid-insoluble,alkali-soluble, hot water-extractable polymer(a PS containing 30% of protein; D fraction)obtained from the fruiting bodies of Grifolafrondosa (Oikawa et al., 1987) exhibited anti-tumor activities against allogenic and syngenictumors after oral administration to mice. The Dfraction was found to potentiate the delayedtype hypersensitivity response which was asso-ciated with tumor growth suppression (Hishidaet al., 1988). CP-MAS C13 NMR spectroscopywas employed to study confirmation of theβ-glucan “Grifolan” (Ohno et al., 1987); amethod for separation and determination of PSfrom Polystictus versicolor was also described(Dong et al., 1989). Structure of the PS consist-ing of D-galactose, D-mannose, and L-fructosewas found to potentiate the delayed-type hy-persensitivity response that was associated withtumor growth suppression (Hishida et al., 1988).CP-MAS C13 NMR spectroscopy was employedto study confirmation of the β-glucan “Grifolan”(Ohno et al., 1987); a method for separationand determination of PS from Polystictusversicolor was also described (Dong et al.,1989). Structure of the PS consisting of D-galactose, D-mannose, and L-fructose isolatedfrom Pleurotus ostreatus was investigated by

using methylation analysis, periodate oxida-tion, mass spectrometry, and NMR spectros-copy (Hranisavljevic-Jakovljevic et al., 1988).PS from extracts of fruiting bodies of Grifolafrondosa were hydrolyzable by α-amylases andconsisted of glucose, galactose, mannose, andrhamnose with small amounts of protein (Katoet al., 1989). A heterogalactan was isolated fromthe fruiting bodies of Agaricus bisporus(Milljkovic-Stojanovic et al., 1986).

PS from Tremella aurantia was unique fromthat of the rest of the seven mushroom speciesstudied, in that mannose constituted the mainsugar (73%); all the PS studied promoted thetransformation of lymphocytes to varying de-grees (Fu et al., 1995). Hot water extracts (con-taining PS) from edible species of Polyporaceaeshowed marked host-mediated anti-tumor ac-tivity; their (PS) chemical modification by mildsmith degradation and products of BH4 reduc-tion after IO4 oxidation enhanced their anti-tumor activity (Mizuno, 1989). I. P. adminis-tration of Maitake D-fraction (a 1,3-branched1,6-β-glucan of molecular weight 106) at 1 mgkg–1 10 times into mice with implanted livercarcinoma gave 90.3 and 91.3% inhibitions ofcarcinogenesis and metastasis, respectively(Nanba, 1995). Heteropolysaccharides from thefruiting bodies of Tremella species containedwater-soluble acidic hyperglycemia inhibitors(Ukai et al., 1995).

Polysaccharides isolated from Agaricusblazei, using vacuum steaming, were found tocontrol viruses in plants and activate plant-physiological processes (Hatsutori, 1987). ThePS extracted from Polystictus versicolor dis-played antiviral (influenza virus) and immuno-potentiating activities in mice (Chen et al.,1986a). Anti-tumor PS (containing about 44%C, and 7% H) from Coriolus were used in acomposition for treating mammalian gas-trointestinal cancer (55 to 90% inhibition rateof tumor growth was observed against Sar-coma-180 cells) (Yoshikumi et al., 1986). Anti-tumor coriolan (molecular weight = 2,000,000)isolated from Coriolus pubescence adminis-tered to mice transplanted with sarcoma-180

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for 14 days totally inhibited the cell growth(Sumio et al., 1986). Glucans from the fruitingbodies of Grifola frondosa displayed anti-tu-mor activity against transplantable Sarcoma-180 (Okuda et al., 1987; Nanba et al., 1987;Adachi et al., 1988). The anti-tumor activity of“Grifolan” was found to depend on not onlydosage but also injection routes and timings(Suzuki et al., 1987). (1-3) (1-6)-β-D-gluco-pyranans of Polyporus confluens (Mizuno et al.,1991), glucans and heteroglucans of Hohen-buehelia serotina (Ma et al., 1991, 1992), cold-alkali extractable β-1,3 glucan (Misaki et al.,1991), and water-soluble 1-3 glucan isolatedfrom Hypsiziqus marmoreus (Ikekawa et al.,1992) had remarkable inhibitory effect againsttumor growth of Sarcoma-180. One of themechanisms of the PS from Coriolus versi-color of its antiviral effect on human immuno-deficiency virus (HIV) was attributable to theinhibition of binding of HIV with lymphocytes.Here the PS was found to inhibit reverse tran-scriptase of avian myeloblastosis virus in anoncompetitive way in vitro. Such inhibitionmay be important in its anti-HIV effect as wellas its inhibitory effect on the binding of HIVwith lymphocytes (Hirose et al., 1987). A pro-tein-polysaccharide produced by extracting themycelium or fruiting bodies of Coriolus withhot water or an aqueous alkali (that contained18 to 38% protein and molecular weight 5000by ultracentrifugal analysis) was useful for treat-ing retroviral infections such as AIDS (Hiroseet al., 1988). Cortinellus shiitake was culturedin a medium containing plant fibers (e.g., ba-gasse), rice bran, wheat bran, and others toproduce an antiviral agent containing proteins2 to 5, sugar 12 to 20, and lignin 70 to 85%.The culture medium was fractionated with etha-nol and chromatographed on Sepharose. Theproduct inhibited the growth of HIV virus on acell culture (Iizuka et al., 1990a). The PS ofCoriolus versicolor enhanced the oxygen me-tabolism of murine peritoneal macrophages andthe host resistance to listerial infection (Saitoand Matsuzaki, 1988). Water-insoluble hetero-glucans from the fruiting bodies of Agaricus

blazei were observed for the host-mediated anti-tumor activity (Mizuno et al., 1990a,b). The PSof Polyporus versicolor inhibited the growthand pulmonary metastasis of melanoma B16 inmice (Hu et al., 1988). Administration of intra-cellular polysaccharide of Polystictus versicolorto rats by I. P injection promoted the clearanceof endotoxin of Escherichia coli from the body.Apparently, such a preparation could enhancebody reticular endothelial system function andis potentially useful for prevention of liver dis-eases (Niu et al., 1986a). Also, the PS waseffective against galactosamine-induced liverdamage (Niu et al., 1986b). Protective effect ofPolyporus umbellatus PS on toxic hepatitis inmice was discerned (Lin and Wu, 1988). Pul-verized mushroom stems were extracted withboiled water followed by precipitation withethanol to yield PS suitable for food (Zhangand Faming, 1992). The nutrient rich in poly-saccharide was prepared from a Lentinus edodesculture broth; medium consisted of starchbase as carbon source and wheat and corngerms, and sesame as nitrogen source (Li et al.,1992).

Several other authors have reviewed thesubject of anti-tumor polysaccharides of mush-rooms (Mizuno, 1989a,b, 1995; Hang et al.,1986).

L. Other Biological UsefulConstituents

A glycoprotein from Coriolus versicolordecreased tumor growth and restored the de-pressed immune function and also increasedsurvival (Tominaga, 1985) in mice. Anti-tumoric proteins having molecular weight of40,000 and 13,000 were isolated from waterextract of Maitake and enokitake by dialysisand ion-exchange chromatography. The anti-tumoric proteins were also useful as anti-hyperlipedemics, anti-hypertensives, and anti-obesity agents (Chihiro, 1996). Protein-boundPS from the culture filtrates of Tricholoma dis-played anti-tumor activity against Sarcoma-180

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(Liu et al., 1995). Mushroom PS-protein com-plexes are described for their mechanism ofaction of anti-tumor activity (Liu et al., 1996).The evaluation of anti-tumor agents bylymphocyte electrophoresis was described(Iwaguchi, 1985). The combined effect of mi-tomycin and glycoprotein of Coriolus versi-color was more pronounced than that of eitheragents alone, for the above-cited functions (Fujiiet al., 1985). A fruiting body protein fromLentinus edodes had a preventive effect on plantvirus (TMV) infection, but no curative effect(Hiramatsu et al., 1987). Preparations from themycelium of Lentinus edodes cultures containedimmunoactive glycoproteins (Toda et al., 1987).Granules of glycoproteins derived fromPolyporus versicolor (for oral formulations,using sucrose, corn starch and hydroxy-propyl-cellulose as adjuncts) were useful for anti-tu-mor activity against Sarcoma-180 in mice (Fujilet al., 1990). Heteroglycan or heteroglycan-pro-tein complexes isolated from the mycelium ofGrifola frondosa reduced tumor growth byactivating the immune system as a biologicalresponse modifier (Zhung et al., 1994). Waterextracts of Pleurotus ostreatus and Lentinusedodes displayed prominent anti-platelet ag-gregation and plasma fibrinolysis acceleratingactivities (Sumi et al., 1996).

6-Deoxyyilludin M, a new anti-tumor anti-biotic from Pleurotus japonicus was weaklyactive against Bacillus subtilis and markedlyactive against murine leukemia (Hara et al.,1987). A novel anti-tumor antibiotic deoxy-coriolic acid from Coriolus species and a novelantibiotic lentiarexine from Lentinus edodesthat was active against Trichoderma andAcremonium were reported (Umezawa et al.,1986; Tokimoto et al., 1988). A lipid fractionfrom Agaricus blazei displayed anti-tumor ac-tivity and macrophage activation (Ito et al.,1986). An extract of the culture medium ofLentinus edodes mycelia caused in vitro inhibi-tion of replication and of the cytopathic effectof human immunodeficiency virus (Tochikuraet al., 1988). 6-Hydroxymethyl-acylfulvene(HMAF-MGI 114) is a novel semisynthetic

anti-tumor agent derived from the sesquiter-pene mushroom toxin illudin-S (Mac Donaldet al., 1997).

Lectins isolated from Agaricus bisporus wereanti-tumor agents (Shiio and Che, 1985). Twocrystalline forms of lectin from Flammulinavelutipes were studied. (Hirano et al., 1987).Lectin from fruiting bodies of Flammulinavelutipes on purification was observed to be adimeric protein, consisting of two identicalsubunits with an apparent molecular mass of11 kDa (Yatohgo et al., 1988). Lectins fromAgaricus bisporus had carbohydrate bindingspecificities (Sueyoshi et al., 1988). A lectinfrom an orange peel mushroom, Aleuriaaurantia was a protein of two identical sub-units having no carbohydrate chain and showedsugar binding specificities for L-fucose(Fukumori et al., 1990, Nagata et al., 1991). Alectin from the fruiting bodies of Ischnodermaresinosum was studied for its chemistry(Kawagishi and Mori, 1991). A galactose-specific lectin from Psilocybe barreraewas isolated and purified (Hernandez et al.,1993).

Twenty species of higher fungi growingin the wild were collected and tested fortheir lectin activities on human, rabbit, andmouse erythrocytes. Fourteen species demon-strated hemagglutination with some erythro-cytes. Of 20 species, eight (Boletus edulis,Boletus splendidus, Clavaria zollingeri,Lactarius subzonarius, Lactarius volemus,Russula cutefracta, Pholiota squarrosa, andPholiota aspera) caused lymphoagglutinationof murine splenic lymphocytes. These eightspecies had more proteins than did the othermushrooms. These species also containedlectins mitogenic toward murine splenic lym-phocytes (Jeune-Chung et al., 1987). A lectinthat was a polymeric protein of several hun-dred kDa consisting of 18-kDa subunits wasisolated from Pholiota aurivella (first isolatedlectin from the family Strophoriaceae). Thelectin agglutinated human erythrocytes, regard-less of blood type and pronase treatment oferythrocytes, equally increased the sensitivity

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to agglutination by lectin (Kawagishi et al.,1991).

A possible role of fractions purified fromLentinus edodes mycelium in treating chronicactive hepatitis was studied in relation to theactivation of host immunity (Suzuki et al.,1986). Antifungal, cytotoxic and antiviral ac-tivities of purines from Collybia maculata weredemonstrated (Leonhardt et al., 1987). Nucleicacid components isolated from Agaricus mush-rooms, displayed anti-tumor activity againstSarcoma-180 in mice (Mizuno et al., 1987).The antimutagenic activity of Flammulinavelutipes and other mushrooms against 3-amino-1,4-dimethyl-5 H-pyrido (4,3-b) indole wasobserved (Ohnishi et al., 1985). Thiazolidine-4carboxylic acid (TCA, thioproline) was a con-densation of cysteine and H2CO. TCA is aneffective nitrite trapping agent in the humanbody and may block endogenous formation ofcarcinogenic N-nitroso compounds. Contentsof TCA in raw fruiting bodies of Agaricusbisporus, Collybia velutipes, Lyophyllumaggregatum, and Tricholoma matsutake were3.8 ppm (Kurashima et al., 1990).

Fused mycelia of Lentinus edodes andCollybia velutipes produced cholesterol-lower-ing and immuno-activating eritadenine (Tanakaet al., 1987). Eritadenine from Lentinus edodes,supplementation in the diet of rats, significantlydecreased plasma concentrations of cholesteroland phospholipids, but not triglycerides(Sugiyama and Yamamkawa, 1996). Hypoli-pidemic principles of wood-rotting mushroomswere not present in the farm grown mushroom,Agaricus compestris (Beyen et al., 1996).Hypocholesterolemic action of Lentinus edodesis evoked through the alternation of hepaticphospholipid composition (Sugiyama et al.,1993). A phospholipid analog containing nonitrogen as an hypertensive agent was extractedfrom Maitake (Grifola frondosa) with organicsolvents (Nanba and Otsuka, 1992). An alco-holic extract of the mushroom Panaeluspapilionaceus (which revealed the presence ofcholine, acetylcholine, tryptamine, 5-hydrox-ytryptamine, 5-hydroxytryptophan and some

unidentified alkaloids and protoalkaloids) in-duced a dose dependent decrease in arterialblood pressure, not associated with a heart ratedecrease in the anesthetized cat (Twaij et al.,1987). The compounds DC 1043 A and DC1043 B from cultures of Pleurotus japonicushad anti-tumor activity against Sarcoma-180(Nakano et al., 1987). An extract of Lentinusedodes containing sugars, minerals proteins, isdescribed for treatment of HIV infection (Iizukaet al., 1990). Intestinal absorption and tissuedistribution of water soluble lignins (derivedfrom cultures of Lentinus edodes) with immuno-modulating in rats, using isotope tracer tech-nique was studied (Hanafusa et al., 1990). Themodified lignins (prepared from mushroomculture base containing sawdust as the majorcomponent to which lignin was added) acti-vated macrophages for immunostimulation andantiviral activity (Iizuka et al., 1993). The cul-tured mycelium of Polyporus confluens wasprocessed to obtain a glyco-protein, useful inpeptic ulcer inhibition (Ito et al., 1991a,b).

Spontaneous hypertensive rats when fedwith a diet containing 5% mushroom (Lentinusedodes or Grifola frondosa) and a 0.5% NaClsolution as drinking water for 9 weeks, showedthe plasma free cholesterol level decreased inLentinus-fed animals, whereas in Grifola-fedanimals, the total cholesterol level decreased.The dietary mushrooms decreased the bloodpressure (Kabir et al., 1987; Adachi et al.,1988a; Jakucs, 1996).

Several more such biologically useful mush-room constituents are listed in Table 24.

M. Toxic Substances

There are only 30 to 50 poisonous speciesamong the thousands of species found on thisearth, and of these, no more than 10 are fatallypoisonous. A wide range of compounds havebeen characterized; some of them have wid-ened the horizons of chemical and biochemicalresearch. Recent advances in the chemistry andbiological activities of these toxic substance,

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160

TA

BLE

24

Med

icin

al a

nd B

iolo

gica

l Pro

pert

ies

of M

ushr

oom

Spe

cies

Spe

cies

Com

pone

ntP

rope

rtie

s/ch

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al n

atur

eB

iolo

gica

l fun

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nR

ef.

Aga

ricus

Lect

in60

,000

— 7

0,00

0 m

ol w

t.;A

gglu

tinat

ed e

qual

ly a

llK

awag

ishi

bisp

orus

stab

le a

t 65

°C;

type

s of

hum

an e

ryth

ro-

et a

l.ca

rboh

ydra

tes

(11%

) cy

tes

test

ed(1

988)

Aga

ricus

Erg

oste

rol

Ant

itum

orM

izun

o et

al.

blaz

eide

rivat

ives

(198

9)A

garic

usG

lyco

prot

ein

Sug

ar (

50.2

%);

Ant

itum

or a

gain

stM

izun

o et

al.

blaz

eipr

otei

n (4

3.3%

)S

arco

ma-

180

(199

0a)

Aga

ricus

An

extr

act

Ash

(5.

54%

), p

rote

inIm

prov

es li

ver

Ito e

t al

.(4

3.19

%),

Lip

id (

3.73

%)

func

tioni

ng(1

990)

crud

e fib

er (

6.61

%)

Sug

ars

(41.

56%

),er

go-s

tero

l (6.

14%

)A

garic

usG

lyco

prot

ein

Yie

ld 7

.5%

of

dry

wei

ght

Ant

itum

or a

ctiv

ityM

izun

o et

al.

blaz

eiof

mus

hroo

ms;

sug

ar 5

0.2%

,ag

ains

t S

arco

ma-

180

(199

0)pr

otei

n 43

.3%

Cor

iolu

sP

rote

in-p

oly-

Inhi

bits

abn

orm

alK

anon

et

al.

vers

icol

orsa

ccha

ride

prol

ifera

tion

of(1

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d ve

ssel

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lus

Pro

tein

bou

ndIm

mun

e en

hanc

emen

tLi

et

al.

vers

icol

orpo

lysa

ccha

ride

50.2

%,in

mic

e(1

990)

Grif

ola

Lect

in f

rom

Gly

copr

otei

n co

ntai

ning

Agg

lutin

ated

all

type

sK

awag

ishi

fron

dosa

mus

hroo

ms

50.2

%,3

.3%

tot

al s

ugar

sof

ery

thro

cyte

s eq

ually

;et

al.

cyto

toxi

c ag

ains

t H

ela

(199

0)ce

llsG

rifol

aC

oppe

r bi

ndin

gM

ol w

t 22

40;

acid

icW

ith p

rope

rtie

s to

bin

d in

Shi

mao

kafr

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sape

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eas

part

ate,

glu

tam

ate,

or t

o m

aint

ain

Cu

in t

heet

al.

serin

e, a

nd g

lyci

neso

lubl

e st

ate

at p

hysi

olo-

(199

3)oc

cupi

ed 8

4% o

f to

tal

gica

l pH

; in

crea

sed

Cu

resi

dues

abso

rptio

nLa

mpt

erom

yces

Lam

pter

o-R

ibof

lavi

nT

he li

ght

emitt

erU

yaku

l et

al.

japo

nicu

sfla

vin

(198

9)Le

ntin

usA

ntib

iotic

2-m

etho

xy-5

-met

hyl-1

,4,

A t

hrom

boxa

ne A

2La

ver

et a

l.ad

haer

ens

benz

oqui

none

rece

ptor

ant

agon

ist

(199

1)

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Lent

inus

Ext

ract

of

Wat

er-s

olub

le li

gnin

s +

Imm

unos

timul

atin

gS

uzuk

i et

al.

edod

esth

e cu

lture

50.2

%,m

inor

am

ount

s of

pro

tein

activ

ity a

nd a

n an

ti-(1

989)

med

ium

(3.2

%)

and

suga

rs (

12.2

%)

HIV

effe

ct in

vitr

oIiz

uka

and

Mae

da,

(198

8)Le

ntin

usE

xtra

ct o

fP

rote

in 2

.5%

, su

gar

12–2

0%,

Ant

ivira

l act

ivity

Iizuk

a et

al.

edod

esth

e cu

lture

Lign

in 7

0–85

%(a

gain

st H

IV)

(199

0)m

ediu

mLe

ntin

usC

ultu

reLi

gnin

65–

75%

; po

lysa

ccha

ride

Inhi

bite

d pr

olife

ratio

nK

oga

et a

l.ed

odes

extr

act

15–3

0%;

prot

ein

10–2

0%of

her

pes

viru

s in

vitr

o(1

991)

and

in v

ivo

Lent

inus

Lign

in d

eri-

Ant

ivira

lS

orim

achi

edod

esva

tives

of

et a

l.cu

lture

med

ium

(199

0)P

leur

otus

Lect

inB

ind

with

gal

acto

seU

sefu

l as

bloo

d co

-H

ashi

mot

oos

trea

tus

or g

alac

tosa

min

eag

gula

tion

fact

oret

al.

(199

0)P

olyp

orus

Cul

ture

Xyl

oglu

can-

prot

ein

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itum

orIto

et

al.

conf

luen

sex

trac

tm

ixtu

re(1

991)

Tirm

ania

Mut

agen

s an

d an

ti-H

anra

n et

al.

pino

ylm

utag

ens

by u

sing

(198

9)di

ffere

nt s

olve

nts

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including the mode of action, are discussed(Konno, 1995). The toxic sesquiterpene Illudin-S was isolated from Omphalotus olivascenscollected in San Diego, California; the yieldwas approximately 5 mg from 400 g of mush-room (McMorris et al., 1989). A hemolyticprotein that causes diarrhoea and death in mice,isolated from the fruiting bodies of Rhodo-phyllus rodopolius was purified (Suzuki et al.,1990).

Structures of hebevinosides I to XI, newmetabolites from the poisonous mushroomHebeloma vinosophyllum were deduced.Hebevinosides I, II, III, V, and VI wereneurotropically and lethally toxic to mice. Theimportant role of glucose at position 16 wassuggested from the investigation on the rela-tion between the structures and toxicities ofthese hebevinosides (Fujimoto et al., 1985,1987). Three metabolites, tentatively namedHS-A, -B, and -C were isolated from Hebelomaspoliatum as fatal toxic principles to mice(Fujimoto et al., 1992). Acromelic acids (verypotent poisonous excitatory amino acids) Aand B from Clitocybe acromelalga were iso-lated, their structure and synthesis elucidated(Konro and Shirahama, 1987). The effects ofacromelic acid, a novel excitatory amino acidfrom the poisonous mushroom, Clitocybeacromelalga, on the crayfish neuromuscularfunction were studied (Shinizaki et al., 1986).

Research on mushroom cyclic peptide tox-ins, mass spectrometry of orellanine, confor-mation of the bicyclic heptapeptide phallacidinof Amanita phalloides using homonucelar 1-di-mensional and 2-dimensional NMR, and con-formational analysis of pallacidin by protonNMR spectroscopy and restrained moleculardynamics were elucidated (Adams et al., 1989;Richard and Ulrich, 1989; Bonzli and Gerig,1989, 1990). Cycloamanide peptides frommushrooms displayed immunosuppressor ac-tivity (Wieczorek et al., 1993).

An HPLC method was used for the deter-mination of amanitin and phalloidin in humanplasma (at 10 ng ml–1 plasma) using the columnswitching technique; and it was an useful

application in suspected cases of poisoning bythe green species of Amanita mushroom(Amanita phalloides) (Rieck and Platt, 1988).Two rapid and very sensitive HPLC methodswere described for the separation and determi-nation of orellanine from Cortinarius orellanus(Cantin et al., 1989).

Bernheimer and Oppenheim (1987) havedescribed the properties of flammutoxin, fromthe edible mushroom Flammulina velutipes. Acytolytic toxin from the basidiocarps of theedible mushroom Flammulina velutipes waspurified to homogeneity. The toxin was a singlepolypeptide chain of molecular weight 32,000and pk approximately 5.4. It contained unusu-ally large amounts of tryptophan, serine, andglycine, and few or none of the sulphur con-taining amino acids. Erythrocytes of rat, rabbit,guinea pig, man, mouse, cat, and dog weresensitive to lysis, in that order, whereas eryth-rocytes of sheep, ox, goat, swine, and horsewere largely or completely resistant to lysis.The toxin appeared not to be a phospholipaseand it was not inhabitable by any of a variety oflipids. Hemolysis probably involved alterationof the erythrocyte membrane, with formationof submicroscopic ion channels, and it appearedto be of the osmotic type. In some respectsflammutoxin resembled phallolysin, cytolytictoxin obtained from the mushroom, Amanitaphalloides. Human amatoxin mushroom poi-soning and advances in therapy are described(Tsuyuki, 1985). An aqueous extract of Amanitapantherina was proved toxic to nervous andkidney systems in mice, but not to the liver(Yamaura and Chang, 1988). Analysis of 10fruiting bodies of Incoybe seruginascens re-vealed a content of the indole derivativeaeruginascin, which was in the same order ofmagnitude as the amounts of psilocybin andbaeocystin. Aeruginascin seemed to modify thepharmacological action of psilocybin to givean euphoric mood during ingestion of the mush-rooms (Gartz, 1989a,b). Hericenone A and Bwere found to be the cytotoxic principles fromHericium erinaceum (Kawagishi et al., 1990a).The cellular protein and DNA syntheses were

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inhibited in the kidney cells by the toxic pro-tein from Boletus satanas; the toxin acted onthe peptidyl elongation step in protein synthe-sis (Kretz et al., 1991). Illudin-S and the in-crease of intestinal propulsion were detectablein methanol extracts from fresh and boiledLampteromyces japonicus, but undetectable inmethanol extracts from slated mushroom(Itagaki et al., 1990). A nephro-toxic substance(orellanine) from Cortinarius speciosissimuswas isolated (Hoimdahi et al., 1987).

The importance of hydrophobicity and sizeof the mono- or bi-pyridines related to themushroom toxin orellanine in the expression oftheir toxicity was confirmed, as well as thepeculiarity of orellanine in the series studied(Richard et al., 1990). Orellanine fromCortinarius orellanus efficiently inhibited thephotosynthetic activity of duck weed (Lemnaminor) at a concentration of 0.04 mM. Anelectrochemical study has shown that orellaninecannot be reduced from NADPH as is methylviologen in animal cells (Richard et al., 1987).The toxicity of orellanine was examined interms of oxidoreduction (Cantin et al., 1988).Pure orellanine extracted from Cortinariusorellanus was highly nephrotoxic in mice, bothwhen given i.p. (LD = 12.5 mg kg–1) or orally(LD50 = 90 mg kg–1) (Richard et al., 1987). Thetoxicities of amanitins, amamins, amanulins,phalloins, phallisins, viroidins, and virosins frompoisonous mushrooms Amanita, Gyromitra,Cortinarius, Paxillus, and Psilocybe were de-scribed (Wieland, 1987). Mushroom toxins-amanitin and phalloidin inhibited hepatopoletininduced 3H-thymidine incorporation into ratliver DNA and production of plasma protein inhepatocyte cultures (Fouad et al., 1987). Lysine-orotate increased the toxicity of amatoxins only,not affecting the toxicity of phalloidins. TLCon silica gel plates and column chromatogra-phy on Sephadex LH-20 indicated the forma-tion of a relatively stable complex of amanitinand lysine-orotate. Thus, lysine-orotate shouldnot be used as a hepatoprotective agent in casesof Amanita intoxication (Halacheva et al.,1988). Cerebroside was isolated from maitake

as the major glycolipid, the principal ceramidewas characterized as N-hydroxypalmitopyl-9-methyltrans-4, trans-8-sphingadienine. Thismolecule was also shown to be distributed inthe fruiting bodies of six other basidiomycetesviz., shiitake, hiratake, tamogitake, enokitake,nameko and tsukuritake (Ohnishi et al., 1996).Oral administration of the toxic mushroom,Cortinarius orellanus to rats caused seriousimpairment of renal function (Prast and Pfaller,1988).

The topic of the hydrazines of toxic mush-rooms and their carcinogenecity is reviewed(Natori, 1987; Toth, 1986). Aortic rupture andaortic smooth muscle tumors were induced byP-hydrazinobenzoic acid hydrochloride ofAgaricus bisporus (McManus et al., 1987). Alarge quantity of agaritine (hydrazine deriva-tive) was detected in fresh Agaricus bisporus,but decreased after boiling the mushroom inwater at 100°C for 10 min. The methanol ex-tract of the fresh mushroom and synthesizedagaritine were suggested to be carcinogens inthe bladder epithelium. Heating mushroomscontaining agaritine before cooking contrib-uted to the prevention of any potential agaritinehazard in the epithelium (Hashida et al., 1990).A survey of various mushroom species showedthat only Agaricus contained agaritine (P-hy-droxy-phenyl-hydrazine) which was reducedby 95% by drying and canning (Stijve et al.,1986). The naturally occurring agaritine wasfound to vary in its concentration with variationsin cultivated strains, size of the fruiting bodyand also the means of processing, reported fromthe UK by Sharman et al. (1990). Agaritine me-diated the mutagenicity of Agaricus bisporusand was not responsible for the mutagenicity ofmushroom extracts (Papaparaskeva et al., 1991).The identity, properties, determination, forma-tion, occurrence, toxicokinetics, short-termmutagenecity tests, and long-term carcinogenic-ity studies of phenylhydrazines of Agaricusbisporus are described (Gry and Pilegaard, 1991).

A technique was developed for the im-proved manufacture of psilocybin and psilocinfrom the fruiting bodies of Psilocybe cubensis

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raised on rice grains; they accounted for 0.95and 0.2%, respectively, of the dried fruitingbodies (Gartx, 1988). A novel procedure wasadopted for extraction of psilocybin andpsiolocin from the fruiting bodies of Psilocybe;the best method was to extract 10 mg powderin 0.5 ml of 50% methanol (saturated withKNO3) and second best method was with 75%ethanol (Kysilka and Wurst, 1990).

N. Enzymes and Co-Enzymes

Mushrooms display a wide capacity to se-crete a number of enzymes of valid propertiesand distinct functions. They are of differenttypes: (1) secreted by the mycelium to biode-grade the growth substrate; (2) those involvedin the transformation of myceloid phase intofructification; (3) those responsible for autoly-sis; besides, there are also other (4) constitu-tive/inductive enzymes characteristic of myce-lium and fruiting body. The ability of mushroomspecies to grow and yield over a wide spectrumof plant wastes is realized only by the secretionand function of these enzymes. It is not surpris-ing to state that the great diversity in shape,size, color, texture, structure, and flavor of thefruiting bodies is an ultimate expression of thephysiology and biochemistry of these enzymes.The genetic system of each species/strain, toregulate and condition the production and for-mation of its own type of mushroom fruitingbodies, despite the availability of a large diver-gent spectrum of chemical substances in thegrowth substrate, is beset with the complexcoordination of sequential production of theseenzymes, that also renders completion of thelife cycle in nature. As more than one kind ofenzyme was dealt in several of these refer-ences, it was difficult to classify them strictlyunder the subtitles.

During a study of the intracellular enzymesin both Chlorophyllum molybditis and Cortin-arius mellionlens, total amylase, α-amylase,proteinase, lipase, peroxidase, catalase, andpolyphenol oxidase activities were increased

with maturity of fruiting bodies than in veryyoung and immature ones. All the enzymesassayed except cellulase and β-amylase showedgreater activity in the pilei than in the stipes.Chlorophyllum molybditis showed greater totalamylase, α-amylase, cellulase, proteinase, cata-lyze, and glucose-6-phosphatase activities thanChlorophyllum mellionlens (Kadiri and Fasidi,1994). CMC-ase, avicelase, β-glucosidase,xylanase, and β-xylosidase were produced byVolvariella volvacea (Cai et al., 1994). Proto-plast preparation and ultraviolet irradiation ofmycelial fragments were used to study the vari-ability of production of laccase peroxidase andmanganese-dependent peroxidase involved inlignin degradation in Pleurotus ostreatus andLentinus tigrinus (Homolka et al., 1995).

Isoenzyme analysis of extracellular laccasesof Agaricus was found to be a promising methodcontributing toward systematic resolution andphylogenetic reconstruction in Agaricus(Kerrigan and Ross, 1988). Eleven enzymeactivities were used, to study the intraspecificrelatedness of Pleurotus species: Pleurotusabalonus, Pleurotus cornucopiae, Pleurotuscystidiosus, Pleurotus dryinus, Pleurotuseryngii, Pleurotus flabelatus, Pleurotusostreatus, Pleurotus pulmonarius, Pleurotussajor-caju, and Pleurotus sapidus. In addition,the zymograms of their homokaryotic prog-enies were evaluated to determine the numberof genes and alleles encoding them (Zervakiset al., 1994).

1. Carbohydrases

An amylase from Termitomyces clypeatusexhibited hydrolytic activity on amylose, xy-lan, amylopectin, glycogen, arabinogalactan,and arbinoxylan (Ghosh and Sengupta, 1987).An amylase preparation from the groundmushrooms of Pleurotus ostreatus, withhigh enzyme activity precipitated with ethanol,followed by freeze-drying, can be used in or-ganic chemistry for the preparation of specificoligosaccharides, and in food industry for the

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production of special syrups and in biotechno-logical applications (Kuniak et al., 1992).

Production of cellulase and laccase byPleurotus ostreatus grown on wheat straw undercontrolled conditions was observed (Giovannozziet al., 1986). Of the 22 strains of Pleurotus,including seven different species, highest activi-ties of exocellular monophenol mono-oxyge-nase and endo-1,4-β-glucanase were observedin Pleurotus pulmonarius and Pleurotusflabelatus, respectively (Semichaeviskii andBisko, 1987).

The biosynthesis and secretion of cellulase(C1 and Cx), xylanase, laccase, and peroxidasewere studied in Bjerkander adusta, grown onsimple salt medium with glucose (Ganbarovet al., 1986a,b). 1-3,β-glucanase, protease, andlaccase were produced during the autolysis ofCoriolus versicolor in fermentor (Gomez-Alarcon et al., 1986). Coriolus hirsutus synthe-sized, cellulase, xylanase, peroxidase, and laccaseon flax scutch as carbon source (Babitskaya andShcherba, 1987). Lentinus edodes producedCMC-ase, avicelase, xylanase, polygalactur-onase, β-glucosidase, and pectin transeliminaseas extracellular wood-degrading enzymes onsawdust medium (Hong et al., 1986). Secretionof lignocellulases on paper-mill sludge byPleurotus sajor-caju (Kanran et al., 1990) andproduction of ligninases, cellulases, hemi-cellulases, oligosaccharidase, proteinases, etc.,from the cultures of Lentinus edodes grown onwood were studied (Leatham et al., 1991).Groundnut shell was able to induce the cellulaseenzyme complex by Pleurotus ostreatus andSporotrichum pulverulentum in liquid or solidstate cultures (Beelman et al., 1989).

The dynamics of formation of CMC-ase, xylanase, laccase, and peroxidase byBjerkandera adusta was largely dependent onthe presence of a suitable substrate inducer(Ganbarov et al., 1986a,b). During solid statefermentation of bagasse, isolates of Polypotusshowed maximum cellulase activities in 4 to 5days and ligninase in 2 to 3 weeks (Nigamet al., 1987). Isozymes of different thermal sta-bility were suggested to be present in the

exocellular cellulases of Coriolus versicolor(Danilyak and Chernykh, 1987). Kinetic andthermodynamic specificity properties ofendoglucanases from the representatives of twoorders of mushroom groups viz., Aphyllo-phorales and Agaricales, were investigated(Danilyak et al., 1989). Thermal treatment notonly significantly stimulated exo- and endo-glucanases, but the enzymes retained their ac-tivity for a significant period, from the twocultures of Polyporus (Nigam and Prabhu,1988). There were differences in activationkinetics of cellobiase and endoglucanase pro-duced from Coriolus hirsutus (Danilyak andKatsan, 1987).

Cellulases from Lentinus edodes on frac-tionation and separation yielded four compo-nents; two had β-glucosidase and CMC-aseactivities, and the other two displayed C1-activity (Xiao and Huang, 1990). A β-gluco-sidase with cellobiase activity from Termito-myces clypeastus was purified to homogenity;the enzyme appeared to be a glycoprotein; op-timum activity was at pH 6 and temperature65°C (Sengupta et al., 1991). β-glucosidaseproduced by the mycelial culture of Termito-myces clypeatus and xylane enzyme of Letinusedodes grown on commercial oak wood me-dium was characterized (Mishra et al., 1990).α-glucuronidase was readily produced by Agari-cus bisporus and Pleurotus ostreatus; the en-zyme acted synergistically with xylanase(s) andliberated 4-O methylglucuronic acid from 4-Omethylglucuronic acid-substituted xylo-oligo-mers (Puls et al., 1987).

Immunogold cytochemical labeling of hy-phal sections of Coriolus versicolor showedthat β-glucosidase was localized in the extra-cellular mucilage, cell wall layers and the cellinterior in hyphae grown on glucose-rich maltextract medium, whereas in hyphae grown withCM-cellulose as sole carbon source, most la-beling was in the cell wall layers, and cellinterior (Gallagher and Evans, 1990). A methodis described for the visualization of exo β-1-3-glucosidase activity in polyacrylamide gel(Vargic and Mnsa, 1994). A review with 36

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references discusses the cellulase production inthe life cycle of Agaricus bisporus (Wood et al.,1988). During the decay of coniferous needlesby several white-rot species, phenol contentwas transformed quantitatively; thereby thebiochemical environment in which cellulolyticenzymes were active had been modified (Savoleet al., 1990). Following UV irradiation of oidia,for the production of cellulase, xylanase, andamylase, this resulted in generation of mutantsin Coprinus bilanatus. Genetic analysis of someof these mutants showed that they were singlegene mutations and were recessive. In crosses,the mutants segregated as predicted, for therandom migration of the nuclei from the ba-sidia into the two spores produced by this sec-ondarily homothallic species (Stephens et al.,1991). Production of major degradative en-zymes on the lignocellulosic wastes, by severalmushroom species is cited in Table 25.

2. Proteinases

Agaricus bisporus, Coprinus cinereus, andVolvariella volvacea when grown on definedliquid media were able to produce proteinases(Kalisz et al., 1987). Metalloproteinase accu-mulated in mycelium after cultivation in thepresence of proteinase inhibitor was the sameas that in the control cultures (Terashita et al.,1980). Absidia blakesleeana and Morchellaesculenta were proven to be the most promis-ing strains for production of protease in liquidcultures on synthetic medium (EL-Zalaki et al.,1995). A proteinase possessing high fibrinolyticand low thrombolytic activities was producedby Clitocybe, Boletus, Coprinus, Fomes, andFomitopsis. Two stable strains of Coprinus wereselected for their potential as industrial produc-ers of fibrinolytic protease (Denisova et al.,1989). Increase in the intracellular activity ofmycelial proteinases was observed during mor-phogenesis in Flammulina velutipes (Chao andGruen, 1987). Protease activity increasedsteadily during cultivation of Pleurotusostreatus on rice and sugarcane straw, withouta marked jump at any stage; the activity stayedlow in the spent straw (Cisneros et al., 1996).

In Flammulina velutipes, metal proteinase hav-ing the isoelectric point pH 6.0 was importantfor the growth of fruiting body and also exhib-ited significant role in basidiospore formation(Terashita et al., 1995). Carboxyl proteinase(s)in the caps of Lentinus edodes were found es-sential for the maturation of basidiospores(Murao et al., 1986). Coprinus atramentariuswas also found to secrete proteinase inactivat-ing enzyme (Otto and Lipperheide, 1986). Pro-pyl endopeptidase (post-proline cleaving en-zyme) from Lyophyllum cinerasceus waspurified and characterized; the high levels ofthis enzyme was also noticed in Agaricusbisporus and Russata lepida (Yoshimoto et al.,1988). A serine proteinase (pro A, EC 3.4 22.9)and 2-metalloendopeptidases (pro B, EC3.4.99.32 and ProC, EC 3.4.24.4) were purifiedto homogeneity from Pleurotus ostreatus fruit-ing bodies. Pro-A was a serine proteinase witha mass of 30 kDa, which had amylolytic andesterolytic activities besides proteolysis andcatalyzed preferential cleavage of the peptidebonds involving the carboxyl groups of hydro-phobic amino acid residues in oxidized bovineinsulin B chain (Dohmae et al., 1995). Oneserine proteinase and two metalloproteinasesfrom a Coprinus species were identified on thebasis of substrate specification and sensitivityto inhibitors (Shaginyan et al., 1989). A thiol-dependent serine proteinase was isolated forthe first time from Coprinus 7N culture filtrate(Shaginyan et al., 1990). Optimum conditionsof culturing Coprinus for the production ofhigh activities of fibrinolytic enzymes inlaboratory and industrial fermentors were stud-ied (Romanovets et al., 1990). Aromatic aminoacid decarboxylase was produced by the culti-vation of Pholiota nameko mycelium (Teradaet al., 1985). Proteases regulated flush coordi-nation in Agaricus bisporus (Burton et al.,1994).

3. Lignin-Peroxidases andManganese-Peroxidases

The sequence of appearance of manganeseperoxidase, lignin peroxidase, and manganese-

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TABLE 25Degradatory Enzymes of Mushroom Species

Mushroom species Enzyme(s) Properties Ref.

Coprinus cinereus Peroxidase Acidic protein, molecular weight Morita et al.41,600 exhibited spectra of a (1988)hemoprotein

Pleurotus ostreatus Peroxidase Glycoprotein containing 35.7% carbohydrate; Bae et al.enzyme is a dimer of identical subunits (1989)(molecular weight = 72,400); contains ironprotoporphyrin; optimum activity at pH 3.5–4.0 and at 40°C.

Trametes versicolor Peroxidase Heme-containing inducible intracellular; Loparzeskiisolated by affinity chromatography on (1987)Vanillin-activated controlled porosityglass column; polymerizes as well as de-polymerizes soluble lignin derivatives; canco-operate with glucose-oxidase in degra-dation of lignocellulosics

Coriolus versicolor Laccase Has 2 Cu atoms per protein molecule believed Morohoshito be necessary for catalysis; molecular (1991)weight of 66,000; acts on lignins to loosentheir three-dimensional structure, permittingdepolymerization and solubilization

Coriolus hirsutus Laccase Molecular mass = 55 kDa; optimum pH Gindilisfor activity 3.5–4.5; catalyzes the electro- et al.reduction of O2 to H2O with a direct electron (1988)transfer from the enzyme active center to theelectrode

Coriolus versicolor Laccase Optimum pH 4.6 and 40°C for activity; stable Hong et al.at 40°C for 30 min; Cu, Fe and Ca activated; (1987)Mn and Hg were inhibitory; totally inhibitedby 1 mM NaN3 and KCN

Coprinus 7 N Proteinase Stable at pH 6–9; optimum activity at 37°C; Shaginyancompletely inactivated by the specific in- et al.hibitors of serine proteinases; hydrolyzes (1990)azocasein, azoalbumin, hemoglobinfibrinin, and synthetic chromogenic peptidesubstrates

Coprinus cinereus Proteinases Chromatographed into 2 fractions — EL and A; Kalisz et al.both had an apparent molecular weight of 31 (1989)kDa; pH 9 and temperature 30°Cfavored the activity of EL; AD was activeat pH 5 and 9 and 56–62°C

Agaricus bisporus Protease Optimum activity at pH 6 and stable at pH 4–7; Eun et al.active at 50°C and instantly inactivated at (1989)60°C; inhibited by Ag, Cu, Ba, Fe, Co, Ca, Pb,Mg, and Mn

Bjerkandera adjusta Aryl alcohol Molecular weight = 78,000; oxidized several Muheimoxidase aromatic alcohols to the corresponding alde- et al.

hydes, simultaneously reducing O2 to H2O2; (1990)pH optimum 3.7, enzyme stable for weeks at 4°C

Pleurotus eryngii Aryl alcohol Catalyzes conversion of primary aromatic Guillenoxidase alcohols to the corresponding aldehydes, et al.

and H2O2; showing no activity with aliphatic (1990)and secondary aromatic alcohols; enzymestable at pH 4–9, temperature 45–50°C; andpH 6–6.5 optima; inhibited by Ag, Pb and NaN3

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independent peroxidase in Coriolopsis poly-zona, Phanerochaete chrysosporium, andLentinus edodes was studied; pyranose-2-oxi-dase was probably the major extracellular H2O2

generating activity with all three species (Vyaset al., 1994a). Two Polyporus species isolatedfrom manure also displayed ligninolytic activ-ity (Nigam et al., 1987).

Disulfide bonds and glycosylation in per-oxidase are reported from Trametes versicolorand Coprinus cinereus (Limongi et al., 1995).Resonance Raman spectra for the resting stateferric and the reduced ferrous forms of recom-binant Coprinus cinereus peroxidase with dif-ferent excitation wavelengths and in polarizedlight were obtained (Smulevich et al., 1994).The lignin peroxidases (Li-p) of Bjerkanderaadusta had immunogenic peptides and tertiarystructures similar to those of the Li-p ofPhanerochaete chrysosporium (Kimura et al.,1994). A three-dimensional structure of a re-combinant peroxidase from Coprinus cinereuswas enumerated (Petersen et al., 1994).

Coriolus versicolor produced an extracel-lular enzyme that resembled the ligninase ofPhanerochaete chrysosporium; its propertieswere described. Similar enzyme was producedalso by Merulius tremellosus (Biswas et al.,1987). Lignin peroxidase was located insidethe fungal cell in Phanerochaete chrysosporiumgrowing on poplar sawdust (Leisola et al.,1987). Lignin peroxidase and xylanase weredetected by immuno-cytochemical labeling inwood decayed by Phanerochaete chryso-sporium, Phellinus pini, and Trametes versi-

color; areas of the wood with early stages ofcell wall decay had the greatest concentrationof gold particles, while little labeling occurredin cells in advanced stages of decay (Blanchetteet al., 1989). A DNA fragment-containing twolignin peroxidase genes (LPG I and LPG II)was isolated from a genomic library of thewhite-rot fungus Trametes versicolor. Strongevidence suggested that LPG I encoded a quan-titative dominant lignin peroxidase isoenzyme,whereas the product of LPG II has not beenidentified to date (Joensson and Nyman, 1994).Trametes versicolor secreted lignin peroxi-dase and manganese peroxidase presumed topartake in lignin degradation. Mn-p genes wererevealed to be different from the peroxi-dase gene of Phanerochaete chrysosporium(Joensson et al., 1994). Li-p oxidizing veratrylalcohol to veratraldehyde and degrading ligninβ-O-4-type dimer containing no phenolic OHgroup and having defined substrate specificitywas manufactured by culturing Coriolushirsutus in liquid medium (Sugiura et al., 1989).Lentinus edodes, strain L 54, produced manga-nese-dependent peroxidase and laccase, but notlignin peroxidase, when grown on a definedmedium with glucose as sole carbon source(Buswell et al., 1995).

4. Phenol-Oxidases

During the secretion of extracellularphenoloxidases by Coriolus versicolor, incu-bated in wood meal medium, the main

TABLE 25 (continued)Degradatory Enzymes of Mushroom Species

Mushroom species Enzyme(s) Properties Ref.

Trametes versicolor Oxidizing Isolated from the culture filtrates; Khan andenzyme induction of synthesis late in the Overend,

growth cycle and does not require an (1991)inducer; pH optimum 3.5; Ferulic acid ando-dianisidine are oxidized

Pleurotus ostreatus Veratryl A glycoprotein with FAD as a prosthetic Sanniaalcohol group; oxidizes cinnamyl alcohol faster; et al.oxidase oxidation of cinnamyl alcohol is slower (1991)

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phenoloxidase fraction decreased in molecularweight with the progress of the decay and aphenoloxidase fraction containing tyrosinaseappeared during the relatively long culture pe-riod of six months (Morohoshi et al., 1989).The occurrence of intra- and extracell-ular polyphenol oxidases (in Coriolus versi-color) were time dependent; the former wassynthesized de novo, and the preferred sub-strate for the latter appeared to be catechol(Moore et al., 1989). Coprinus cinereus pro-duced a developmentally regulated phenol-oxidase that appeared to be responsible for theblack pigmentation of basidiospores (Vnenchakand Schwalb, 1989). There appeared to be arelation between the time-dependent appear-ance of phenol oxidase and catechol enhancedmycelial growth in Coriolus versicolor (Tayloret al., 1987).

Immobilization of phenoloxidase by entrap-ment in an alginate gel was described (Palmieriet al., 1994). Their role in photomorphogenesisin Coprinus congrigatus (Choi, 1987), as wellas their production and immobilization (Cho,1991) were considered.

Two methods viz., oxidation of veratrylalcohol to its aldehyde and decolorization ofthe dye Remazol Brilliant Blue R, were evalu-ated comparatively for measuring ligninaseactivity in Coriolus species (Chernyagin et al.,1991). In contrast to species of Polyporus nolaccase, lignin peroxidase or poly B-411 oxi-dase could be detected in cultures of Schizo-phyllum commune; however, both the fungieffected the same range of lignin demethylation(Trojanowski et al., 1986). In Pleurotus sajor-caju, crude extracellular ligninolytic enzymesreduced the brown color of the chlorinated oxy-lignin and crude cell wall enzyme decolorizedP-nitroso-N,N-dimethyl-aniline (Fukuzumi,1987).

A model was proposed to explain howoxidation of carbohydrate and reduction ofmanganese dioxide and quinones, by cellobiosequinone oxido-reductase, might complementoxidation by manganese peroxidase, thus pro-moting lignin biodegradation (Roy et al., 1994).

FAD-dependent veratryl alcohol oxidase (VAO)from Pleurotus ostreatus was able to reducesynthetic quinones, laccase-generated quinoidsand phenoxy radicals with veratrylaldehyde.This cooperation in action of laccase and alsoVAO prevented the polymerization of phenoliccompounds and reduced the molecular weightof soluble lignosulfonates to a significant ex-tent (Marzullo et al., 1995). In Pleurotuseryngini, a multienzyme cyclic system is pro-posed, in which H2O2 was produced extracellu-larly by the action of aryl-alcoholic oxidase onbenzyl alcohol, the most abundant compoundafter redox reactions (Guillen et al., 1994). Aryl-alcohol oxidase and dehydrogenase activitiesin a number of species of Pleurotus were pro-posed to be involved in the redox-cycling ofthe aromatic compounds providing H2O2 toligninolytic peroxidases (Gutierrez et al., 1994).An oxygenase from Trametes versicolor re-duced sinapic acid esters in canola meal (Lackiand Duvnjak, 1994).

The influence of the growth of two white-rot fungi, Pleurotus ostreatus and Lentinusedodes, on the digestibility of corn straw (Zeamaize) was evaluated. Pleurotus ostreatus andLentinus edodes showed a different pattern ofrelease of extracellular enzymes, includingphenol-oxidases, cellulases, and xylanases. Thebest results, in terms of delignification and in-crease in digestibility, were obtained in Lentinusedodes cultures. When Pleurotus ostreatus andLentinus edodes were grown in submerged fer-mentation conditions in the presence of a watersoluble lignin-rich copolymer, a crude filtratecontaining phenol-oxidases but not cellulolyticenzymes was obtained (Sermanni et al., 1994).Production of extracellular laccases was re-ported for Polyporus versicolor and Pleurotusostreatus (Claus and Filip, 1990). Addition ofsunflower oil to the growth of Pleurotusostreatus in submerged culture increased thelaccase activity, but inhibited endoglucanase(Schiesser et al., 1989b). Laccase secretion byTrametes versicolor and Pleurotus sajor-cajuwas affected by ferulic acid at 5 mg l–1 (Asiegbuet al., 1996b). Laccase purified from culture

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broth of Pleurotus ostreatus mycelium was asingle protein of molecular weight 59,000 andwas active on O-diphenyl substrates (Sanniaet al., 1986). Laccase-type phenol oxidases werethe principal oxidative enzymes secreted byTrametes (Coriolus) versicolor. These laccasescould oxidize, polymerize, and, under someconditions, cleave a wide variety of biologicaland synthetic phenolic compounds. Each of thefungal laccase proteins tested could rapidlypartially dechlorinate a number of toxic poly-chlorinated phenols and guaiacols (Roy-Arcandand Archibald, 1991). Laccase fractions fromCoriolus versicolor able to degrade lignin werefractionated by ion-exchange chromatographyand preparative focusing. The fractionated peakshad different enzyme activities and substratespecificities (Morohoshi et al., 1988a,b). Alaccase (180 mu. L.o/h/g wet weight) was manu-factured by extraction from the fruiting bodiesof Agaricus bisporus (Higashiura et al., 1989).Demonstration of laccase activity in Gloeo-phyllum trabeum and several other brown-rotfungi was of particular interest because theseorganisms were not previously shown to pro-duce laccases (D’Souza et al., 1996). The ef-fects of clays and other solids typical for soiland ground water environments, on the activityof laccases produced by Polyporus versicolorand Pleurotus ostreatus were studied. The lim-its for the in situ microbial production of phe-nol oxidases were indicated (Claus and Filip,1990). Laccase from Coriolus versicolor wasisolated and its immobilization was achieved.(Rogalski et al., 1990). A laccase of Trametesversicolor was immobilized on porous glassbeads that were activated with 3-aminopropyltriethoxysilane and glutaraldehyde. The immo-bilized enzyme was found reusable in treatingdifferent substrates, either recycled alone or ina sequential order (Leonowicz et al., 1988).Such an immobilization resulted in an enzymewith much higher stability and reusability. Theenzyme was also less sensitive to higher tem-peratures than the free enzyme. In the future,such an immobilized enzyme may be used todetoxify environments that have been polluted

with phenolic derivatives of agricultural or in-dustrial origin. 2-4-Di (tert-butyl)-4-(methoxy-carbonylmethy1)-2-buten-4-oilde was formedas an aromatic ring cleavage product of a phe-nolic lignin model compound, 4-6-di (tert-butyl)guaiacol, by laccase of Coriolus versicolor(Kawai et al., 1988b). Maximum relative ac-tivities of Pleurotus eryngii, Pleurotus osteatus,Pleurotus sajor-caju, and Pleurotus sajor-cajuA, were 10, 6.7, 6.0, and 3.0 units, respec-tively, for laccase and 8.0, 5.6 4.8, and 3.0 unitsfor peroxidase (Fiskin et al., 1989). Laccase ofTrametes versicolor was able to transform trans-4-hydroxycinnamic acid (Katase and Bollag,1991). Sites of copper in laccase of Polyporusversicolor were studied (Hanra, 1988).

α-, β-bond cleavage of syringyl glycerol-β-guaiacyl ether was the initial and major reac-tion of laccase III from Coriolus versicolor,which was one of the important ligninolyticenzymes attacking free-phenolic units (Warishiet al., 1987). Regulation of laccase activity fromCoriolus versicolor in the surfactant-water-or-ganic solvent system modelling lipid polymor-phism of biomembranes was enunciated(Pshezhetskii et al., 1987). A possible pathwayof lignin biodegradation was shown while study-ing the properties of laccase from Pleurotusostreatus and Coriolus versicolor, and metha-nol oxidase from Sporotrichum pulverulentum(Nishida et al., 1987). A laccase preparationfrom Pleurotus ostreatus was able to catalyzesingle electron transfer with the formation ofthe phenoxy radical as an intermediate (Younet al., 1995). A reduction-oxidation cycle wasproposed for the functions of laccase andveratryl alcohol oxidase in depolymerizationof lignin phenolic substructures (Bourbonnaisand Paice, 1989). Laccase (oxidation-reduc-tion enzyme) isolated from Trametes versicolortransformed lignin preparations solubilized ina dioxane-water (7:3) mixture, resulting in lig-nin co-polymerization (Milstein et al., 1994b).

A laccase from Trametes versicolor wasimmobilized on porous glass beads that wereactivated with 3-amino propyl-triethoxysilaneand glutaraldehyde. The immobilized enzyme

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was found reusable in treating different sub-strates, either recycled alone or in a sequentialorder (Leonnwicz et al., 1988). A new proce-dure was developed for entrapment of an abun-dantly produced laccase from Pleurotusostreatus, by entrapment in copper-alginate gelresulting in an increase of the stability andactivity of the immobilized enzyme. Utiliza-tion of the enzyme for the removal of toxicphenolic compounds from oil mill waste wa-ters was exploited (Sannia et al., 1994).Amperometric biosensors based on poly-phenoloxidase using mushroom tissue sliceswere developed as a novel tool to determinephenolic compounds (Canofani et al., 1994).An aeration rate of 0.5 vvm, an agitation speedof 400 rpm, and pH control 4.0 in a jar fermen-tor were able to increase the mycelial dry weightand the polyphenol oxidase activity by Coriolusversicolor to 105 U ml–1 in 7 days (Yoshiyamaand Itoh, 1994). The phenoloxidases secretedfrom Coriolus versicolor in the solid culturewere different from those in liquid culture,quantitatively and qualitatively. Liquid cultur-ing favored production of stronger enzymeactivities (Morohoshi et al., 1988a,b). Measure-ments of residual enzyme activity and FTIRspectroscopy revealed that mushroom polyphe-nol oxidase is a thermosensitive enzyme readilyinactivated by temperatures exceeding 50°C.The enzyme is however, very pressure stable(Weemaes et al., 1997). Phenoloxidase produc-tion appeared to be highly stimulated, whenLentinus edodes and Pleurotus ostreatus weregrown on whey permeate, a dairy product (DiLena and Giovannozzi, 1994). A phenol-oxi-dase fraction isolated from the extracellularcrude enzyme of Coriolus versicolor had thefunction of depolymerizing lignin in wood resi-dues (Morohoshi and Haraguchi, 1987a,b).Several mushroom species were also observedto produce phenol oxidases (Garibova et al.,1987; Koide et al., 1986). Pleurotus ostreatusactively synthesized laccase, peroxidase, lig-nin peroxidase, polyphenol oxidase, and Mn-dependent peroxidase (Akhmedova, 1995).Coprinus cinereus cultured in a potato-sucrose

medium for 1 week at 25°C produced peroxi-dase (Terada et al., 1986a). An extracellularperoxidase capable of degrading lignin modelcompound was isolated from nonoxygenatedstationary cultures of Coriolus versicolor un-der conditions of carbon limitation, with theaddition of veratryl alcohol as inducer (Dodonet al., 1987). The peroxidases of Coriolus ver-sicolor were excreted, when the carbon sourcein the medium was limited and veratryl alcoholwas added to the medium as an inducer of theenzyme. In a medium with limited nitrogen,the enzyme was excreted to the greatest extentwithout addition of veratryl alcohol (Morohoshiet al., 1990). Peroxidases from Trametes versi-color in lignin biotransformation are reviewed(Lobarzewski, 1990). Production of extracellu-lar peroxidase in Bjerkandera species strain BOS 55 as secondary metabolic event, was trig-gered by carbon limitation (Mester et al., 1996).Limitations of the lignin peroxidase system fromPhanerochaete chrysosporium were observeddue to its inability to degrade two recalcitrantaliphatic ether compounds, high-molecular masspolyethylene glycol (PEG 20,000) and methyltertiary-butyl ether; structural features of sub-strate molecules might be requisite for oxida-tion by the enzyme (Kay-Shoemake andWatwood, 1996). The reaction of lignin per-oxidase of Phanerochaete chrysosporium,modified with aliphatic acid, was found to de-pend on the viscosity of the reaction systemcontaining 70% water-miscible organic solvents(Yoshida et al., 1996). Yields 0f 3600 µ l–1

were produced after 95 h of incubation, (indi-cating significant productivity for industrialpurposes 900 µ day–1 l–1). When Mn-peroxi-dases were overproduced by Phanerochaetechrysosporium, the enzyme was immobilizedon nylon net in a bubble column reactor (abioreactor design of compromise between apneumatic reactor and an immobilized biofilmreactor) (Laugero et al., 1996).

The production of laccase and peroxidasewas stimulated when Coriolus versicolor wasgrown in the vinasse (waste water of alcoholfermentation processes); maximum activities

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were recorded on the 16th day in the mediumcontaining 10% vinasse (Yesilada et al., 1991).The cultural requirements favoring productionand properties of lignin peroxidase by Coriolushirsutus were described (Sugiura et al., 1989).Peroxidase similar to HRP, was purified andcharacterized from a culture broth of Coprinuscinereus (Morita et al., 1988). Peroxidase fromCoprinus cinereus was observed to find use inthe estimation of lipid peroxidase in the serumfrom hyperlipidemia patients (Suntory, Ltd.,1990). Mushroom tyrosinase activity was in-fluenced by phosphonic analogs of tyrosine(Straatsma and Bruinsma, 1986). Tyrosinaseseemed to be the major phenol oxidase in thestrains Agaricus, while oyster and shiitakemushrooms had much lower levels (Khan andAli, 1987; Ratcliffe et al., 1994). Interaction ofthe mushroom tyrosinase with the plasma mem-brane might give protection from proteolyticattack (Miranda et al., 1989). Tiron was de-scribed as a substrate for mushroom tyrosinase(Kahn and Miller, 1987). Tyrosinase was se-creted from three strains of Agaricus bisporuswith L-DOPA as substrate (Moore and Flurkey,1989; Kahn, 1990). Oxidation of sinephrine(Garcia-Carmona et al., 1987) and oxygenationof fluorinated tyrosines to release fluoride ionby mushroom tyrosinase were recorded (Phillipset al., 1990). An efficient oxidative C-C cou-pling by mushroom tyrosinase of hinderedphenols led to diphenoquinones and bisphenols(Pandey et al., 1990). Mushroom tyrosinase wasinactivated with reducing agents such as H2O2,ascorbic acid, phenyl hydrazine, gallic acid,ferrocyanide, and ammonium hydroxide (Yang,1989). The catecholase activity of tyrosinaseextracted from freeze-dried mushroom powderwas reversibly inhibited by CO (Albisu et al.,1989). Benzoic acid inhibited the catecholaseand cresolase reactions of the α-, β-, andgamma-isoenzymes of Agaricus bisporus tyro-sinase (Menon et al., 1990). Maltol (3-hydroxy-2-methyl-4H-pyran-4-one) did not inhibit tyro-sinase activity per se but only gave an apparentinhibition, probably due to its ability to conju-gate with O-quinones (Kahn et al., 1994).

Through a spectrophotometric method, the ki-netic differences among the two activities(cresolasic and catecholasic) of mushroom ty-rosinase was investigated in the pH range 4.9-7.5 and in the presence of metal ions of biologi-cal interest such as Zn, Cd, Co, Cu, Mn, Se, andNi (Vanni et al., 1990). The kinetic propertiesof six tyrosinase isozymes purified from thebrowned gill of the fruiting body of Lentinusedodes differed greatly according to whetherthey contained β- or gamma-polypeptide, indi-cating these polypeptides to be a possible regu-latory subunit (Kanda et al., 1996). 2,4,5-THBP(2,4,5-trihydroxybutyrophenone) was a sub-strate for mushroom tyrosinase with a Km valueof 1.0 mM. The intermediate product was 2,4,5-THBP-quinone that was converted to colorlesspolymerized 2,4,5-THBP-OH, which then wasoxidized to a red polymerized 2,4,5-THBP-quinone(s), the final red product(s) (Kahn et al.,1991). Mushroom tyrosinase was observed tofind use as an oxidant for the synthesis of 5,6-dihydroxyindole derivatives (Lim and Patil,1987).

Mushroom tyrosinase could be sensitivelyassayed using DOPA (Schmidt, 1990). Mush-room tyrosinase was absorbed on a carbon pasteelectrode, as an amperometric biosensor forphenols (Skladal, 1991). A mushroom tissue-carbon paste electrode was used for ampero-metric measurements of inhibitors of tyrosi-nase. Measurements are carried out in thepresence of the catechol substrate. The influ-ence of tissue loading and location in the plantare explored, and possible response mecha-nisms are discussed. The resulting inhibitorbiosensor is inexpensive, characterized by highsensitivity and speed, offers micromolar detec-tion limits, and requires no incubation period(Wang et al., 1996). A sensitive electroanalyti-cal method was described for the determinationof phenol in the presence of mushroom tyrosi-nase (Rivas and Solis, 1994). The reactionbetween 4-tert-butylphenol and mushroom ty-rosinase was investigated by following 4-tert-butyl-ortho-benzoquinone formation, whosehigh stability permits the reaction to be used as

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a model for the study of the monophenolaseactivity of tyrosinase (Ros et al., 1994a). Hy-droxylase and dehydrogenase activities of ty-rosinase-II from Agaricus bisporus were char-acterized (Papa et al., 1994a,b). The transientphase of tyrosinase activity acting on mono-phenols was investigated (Ros et al., 1994b). Acontinuous spectrophotometric method was de-veloped for the rapid determination ofmonophenolase activity of tyrosinase. Thismethod was based on the coupling reactionbetween 3-methyl-2-benzothiazolinone hydra-zine and the quinone products of the oxidationof various monophenols in the presence of ty-rosinase (Rodriguez-Lopez et al., 1994). Mush-room tyrosinase catalyzed synthesis ofcourmestans, benzofuran derivatives, and re-lated heterocyclic compounds (Pandey et al.,1989). The pH-dependent changes in the ki-netic properties of mushroom tyrosinase (Deviet al., 1989) and difference in isoenzyme pro-file of mushroom tyrosinase with developmen-tal stages of mushrooms were investigated(Flurkey, 1991). Mushroom tyrosinase couldbe purified and characterized using inhibitors,phenolics, alkyl groups, and antibodies coupledto solid supports (Ingeebrigtsen and Flurkey,1988). The effects of glutathione, cysteine andascorbic acid on the monophenol and diphenoloxidase activities of mushroom tyrosinase wereassessed by HPLC with electrochemical detec-tion at both oxidative and reductive potentials(Nappi and Vass, 1994). Histochemical stainedareas (of live mushroom slices) for tyrosinasewere present throughout the entire tissue, butthe gills, stalk, and cap epidermis showed darkerstaining reactions (Moore et al., 1988). Modifi-cations (for preparation of tyrosinase) viz. (1)enzyme recovery by performing pellet reex-tractions, (2) preparative isoelectric focusingpurification replacing a gel permeation, and (3)use of polyvinyl pyrrolidione to remove con-taminant brown proteins (instead of basic leadacetate) was found to result in enhancing theamount of tyrosinase recovered, and, thus, re-ducing the quantity of mushrooms required(90% less) (Papa et al., 1994a,b).

5. Oxido-Reductases and Pyranose-Oxidases

The stereospecificity of NAD(P) H oxida-tion catalyzed by 4-aminobenzoate hydroxy-lase from Agaricus bisporus was examined(Tsuyl et al., 1989). The action of glucose oxi-dase in reducing quinone improved the effi-ciency of lignin depolymerization by Trametesversicolor (Szklarz and Leonowicz, 1986). Botharyl alcohol oxidase and lignin peroxidase werepurified from ligninolytic cultures of the white-rot fungus Bjerkandera adusta (Muheim et al.,1990b). An oxygenase enzyme system fromTrametes versicolor was capable of attackinglignin and a large number of di- and tri-substi-tuted benzene rings containing at least onehydroxy group. This enzyme was produced latein the growth cycle without the requirement forany inducer (Khan and Overend, 1990). Thecomplex of oxido-reductases of Coriolushirsutus was immobilized on fibrous supports(Vol’f et al., 1986).

Conditions for production and propertiesof pyranose oxidase from Polyporus were evalu-ated (Uchida et al., 1995). A glucose-specificpyranose oxidase produced by Coriolus,Daedaleopsis, Gloeophyllum or Pleurotus isuseful for enzymic determination of glucoseand of substances or enzymes yielding glucoseas a reaction product (Nakanishi and Machida,1987). The glucose electrode (as glucose sen-sor) was constructed by combining an oxygenelectrode and pyranose oxidase immobilizedon cellulose acetate membrane. The assay takes40 to 50 s and the sensor showed good stabilityat room temperature (~70 days without deterio-ration in its response) (Suye and Inuta, 1991).

6. Other Enzymes

Esterase isoenzyme patterns were quite dif-ferent between mono- and dikaryotic myceliain (conducted from 58 accessions of) Lentinusedodes; malate dehydrogenase, glutamate de-hydrogenase and alcohol dehydrogenase pat-

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terns were not (Li and Zhang, 1988). Severaldehydrogenases of 11 isolates from 6 speciesof Pleurotus were characterized for an electro-phoretic pattern. Besides intercompatibilitiesand morphological features, employing an in-dex of similarity based on relative mobilities ofthe enzyme bands is projected to be useful inanalysis of species relation (Magae et al., 1990).The mannitol dehydrogenase purified fromAgaricus bisporus was used for the determina-tion of D-mannitol and also the D-mannose con-tent of glycoproteins and polysacchrides fol-lowing the liberation of that hexose andreduction to D-mannitol (Berenzenko and Stur-geon, 1991).

The white-rot fungus Trametes versicolordegrades lignocellulosic materials at least inpart by oxidizing the lignin via a number ofsecreted oxidative and peroxidative enzymes.An extracellular reductive enzyme, cellobiosedehydrogenase (CDH), oxidizes cellobiose andreduces insoluble Mn (IV) O2, commonly foundas dark deposits in decaying wood, to form Mn(III), a powerful lignin-oxidizing agent. CDHalso reduces ortho-quinones and produces sugaracids that can promote Mn-P and thereforeligninolytic activity (Roy et al., 1996). Twoallelic variants were found to encode cello-biose dehydrogenase from Phanerochaetechrysosporium (Li et al., 1997).

Activities of trehalase and glycogen phos-phorylase were determined for stage 1 (pin)sporophores of Agaricus bisporus harvesteddaily throughout several fruiting cycles(flushes). Both enzymes exhibited maximumactivity, co-incident with peak flush as definedby maximum yield of stage 2 to 4 sporophores,and minimum activity during the interflushperiods. Glycogen phosphorylase activity some-times peaked on more than one occasion dur-ing a flush, whereas trehalase showed only asingle peak of activity per flush. These resultsare discussed in relation to metabolic eventsassociated with carbohydrate changes duringthe periodic fruiting cycle of this mushroom(Wells et al., 1987). Trehalase from Agaricusbisporus was separated, fractionated and

showed optima of pH 6.0 and temperature 40°C(Lee and Kim, 1986). A novel type of trehalosephosphorylase was found in Flammulinavelutipes. The enzyme catalyses both the re-versible phosphorylysis of trehalose to formα-glucose-1-phosphate and glucose and alsothe synthesis of trehalose. Comparison of thespecific activity of trehalose phosphorylase withthat of trehalase suggested that the function ofthe former enzyme was more important in thefruiting bodies (Kitamoto et al., 1988).

The superoxide dismutase isoenzymechanges, during storage in Volvariella volvacea,were related to the possible mechanism of se-nescence (Li and Zhu, 1987). An enzyme lyasefrom Lentinus edodes catalyzed the hydrolyticcondensation of two molecules of a S-substi-tuted L-cysteine sulfoxide to form a disulfidewith release of ammonia and pyruvate(Yasumoto and Iwami, 1987). It is suggestedthat an endogenous flavo-protein served as thephotoreceptor for blue light activation of themitochondrial ATP synthase in Lentinus edodes(Park and Min, 1991). Activities of the F1-ATPase purified from Lentinus edodes werestimulated by Fe3+, Mg2+, K+, and CO2+, butwere inhibited by Zn3+, Ca3+, Cu2+, and Ni2+,ions (Min and Park, 1991). A novel type ofascorbate oxidase was purified 420-fold fromthe cytosolic fraction of the mycelia of Pleurotusostreatus with an overall yield of 13%. Theenzyme is a hemoprotein, quite similar to b-type cytochrome, and contains 2 mol of hemeper molecule. The reaction catalyzed by theenzyme was L-ascorbic acid + O2 → dehydro-L-ascorbic acid + H2O2 (Kim et al., 1996b).

The first linkage map of 19 alloenzymeencoding loci for the Pleurotus genome waspresented (May et al., 1988). Molecular char-acterization was reported for a gene coding fortryptophan synthetase in Coprinus cinereus(Skrzynie et al., 1989). The RNA-ase and DNA-ase enzymes were assayed from fresh fruitingbodies of Flammulina velutipes (Kurosawaet al., 1990). Application of recombinant DNAtechnology for production of wood-degradingenzymes of Coriolus versicolor is reviewed

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with 19 references (Williams et al., 1990).Evolution of 3 species of Pleurotus — Pleurotusflorida, Pleurotus ostreatus, and Pleurotussapidus, was traced by a comparison of theirisoenzymes of malate dehydrogenase, malicenzyme and tetrazole oxidase (Huang et al.,1987). Proline iminopeptidase from Pleurotusostreatus can be used for removing the bitter-ness from food, such as soy proteins (Yoshimotoet al., 1991).

NADP-GDH and glutamine synthetase inthe mycelium of Agaricus bisporus were re-pressed when grown on NH4, whereas NAD-GDH activity was 10 times higher; activities ofthe former two were derepressed whenglutamate was used as the N source. Regula-tion of these enzymes in the presence and ab-sence of other N and C sources was studied(Baars et al., 1995b). The reproductive processof Lentinus edodes observed to start by the20th day of incubation stimulated glutamatedehydrogenase activities in the early growthstages, in the presence of phenolic compoundsand uronic acids, and may be responsible forthe induction of formation of fruiting bodies(Ikegaya et al., 1994).

Agaricus bisporus has the enzymic poten-tial to assimilate ammonia by the activities ofglutamine synthetase, NAD-, and NADP-de-pendent glutamate dehydrogenases. It also con-tains glutamate synthetase and a number oftransaminating activities such as glutamate-ox-aloacetate transaminase, glutamate-pyruvatetransaminase, and alanine-glyoxylate transami-nase. The specific activities of the ammoniaassimilating enzymes showed no variation dur-ing maturation of the fruiting bodies (Baarset al., 1994). Oxalate decarboxylase was de-tected both intra- and extracellularly in liquidcultures of Coriolus versicolor. Immunogold-cytochemical labeling of ultrathin sections ofthe degraded beach wood showed that the en-zyme was located close to the plasma mem-brane and in intracellular vesicles (Dutton et al.,1994). Highest levels of ammonia assimilatingenzymes viz, NAD-dependent glutamate dehy-drogenase and glutamine synthetase were found

in the fruiting bodies of Pleurotus ostreatus(Mikes et al., 1994).

A guanine nucleotide-specific RNA-ase wasisolated from the fruiting bodies of Pleurotusostreatus (Nomura et al., 1994). An oxalatedecarboxylase was purified from the fungusCollybia velutipes, and the gene encoding itwas cloned for expression in plants. The genewas introduced into tobacco by Agrobacterium-mediated transformation, and the activity de-tected in regenerated plants by assaying foractivity (Datta et al., 1994). Several other en-zymes of mushroom species are depicted inTable 26.

O. Various Other Compounds

Besides the above synthetic capacities, anumber of mushroom species are known togenerate a great diversity of compounds formedas metabolites during their growth. Several ofthem are known to bear useful functions.

Glucose (1%) and peptone (0.05%) in thegrowth medium at 25°C and pH 5.5 favored thebiosynthesis of trehalose by Pleurotus sajor-caju and Pleurotus ostreatus; maximum yieldof trehalose was obtained after 10 days of cul-turing (Hong et al., 1987b). Tryptophan de-rivatives were produced by culturing Psilocybe,Panaeolus, Inocybe, Conocybe, and Pluteus onsolid media (Gartz, 1990). “Natural” methyl-anthranilate was manufactured by N-demethyl-ation of di-methylanthranilate with Trametes,Polystictus or Polyporus in shake flasks (Pageet al., 1989). Methyl-p-methoxycinnamate andmethyl-p-methoxybenzoate were produced un-der nitrogen limited culturing of the brown-rotfungus, Lentinus lepideus (Ohta et al., 1990).Two types of O-methyltransferases were in-volved in the biosynthesis of secondary me-tabolites in Lentinus lepideus mycelium (brown-rot fungus), which catalyzed the formation ofmethyl esters of free cinnamic acids and p-methoxybenzoic acids.

A new method for the purification of mela-nin extracted from Tuber melanosporum with

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TABLE 26Other Enzymes of Mushroom Species

Mushroom Species Enzyme(s) Properties Ref.

Agaricus bisporus Glutamate NADP-dependent; key enzyme in NH3 Yamamotodehydrogenase assimilation; molecular weight 330 kDa; et al.

Isoelectric point at pH 4.8; pH optima for (1986)amination and deamination were 7.6 and9.0; optimum activity at 33°C

Agaricus bisporus DNA Purification yielded 3 bands of 72, 65, and Llerenapolymerase 36 kDa; optimum activity at pH 7.8 in the et al.

presence of 5 mM Mg and 50 mM KCL at (1987)28–30°C; found only in the meiotic cellrich fraction

Agaricus bisporus Propyl endo- Enzyme was most active at pH 7.5 and stable Sattarpeptidase in the range of pH 5–9, when checked with et al.

Z–Gly–Pro–beta–napthylamide (1990)(Z = N-benzoxycarbonyl)

Collybia velutipes Oxalate Fraction A of the 2 purified fractions was Dodsondecarboxylase 1670-fold; had a Km of 4.5 mM for et al.

potassium oxalate; inhibited by PO4 (K i for (1987)PO4 = 9 mM); optimum pH at 3.0

Coprinus cinereus Endonuclease Purified from basidiocarp tissues; its Sakaguchipeak activity appears during the meiotic (1991)prophase; optimal pH 8.3 and temperature50°C; contains a single 43 kDa polypeptide;converts the supercoiled DNA to relaxed DNA

Flammulina velutipes Phosphodies- Considered to function in vivo as anterase oligonucleotidase, which efficiently

converts oligonucleotides to 51-mononucleotides in the cell

Flammulina velutipes Trehalose Catalyzes both the reversible phosphorlysis Kitamotophosphorylase of trehalose to form d-glucose-l-phosphate et al.

+ glucose and also synthesis of trehalose (1988)(the latter is more important in thefruiting bodies).

Flammulina velutipes Nicotinamidase Activity optimum at pH 7.3 and at 45°C; Taguchiactivation energy 10.96 Kcal molecule–1; et al.nicotinaldehyde, 3-cyanopyridine, nicotinic (1989)acid hydrazide; pyrazinamide, benzamide arecompetitive inhibitors

Lentinus edodes DNA topoiso- Molecular weight 71,500; no energy factor Kono et al.merase was required; activity enhanced 10 folds (1986)

by Mg++ and 8 folds by KCLLentinus edodes Mitochondrial Stimulated by 680 nm illumination; optimum Min et al.

ATP-ase pH 7.5; temperature 59°C; enzyme was (1987a,b)inhibited by 5 m mol Na+

Lentinus edodes Acid Stable at pH 4; 60°C; activity markedly Sawada andphosphatase inhibited by NaF, K2Cr2O7, Na2M0O4, Endo,

and Na2NO4 (1987)Lentinus edodes RNA-ase Molecular weight 21,000; one of the Shimada

base nonspecific and adenylic acid et al.preferential RNA-ases such as RNA-ase (1991)T2, RNA-ase Rh and RNA-ase M

Lentinus edodes Aryl-alkyl Purified from wheat bran culture; molecular Kofujitaoxidase weight 65,000 oxidizes guaiacol, O- and et al.

p-phenylenediamines, syringaldazine, (1991)catalyzes alkyl-aryl cleavage

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TABLE 26Other Enzymes of Mushroom Species

Mushroom Species Enzyme(s) Properties Ref.

Lentinus edodes Branched Isoenzyme II; mol wt.=72,000; N-terminal Min et al.chain amino acid glycine; optimum pH 8.2 and (1992)amino acid temperature 38°C; stable at 20°C fortranferase 30 min; activity on L-leucine as substrate;

inhibited by hydroxylamine, N-ethylama-leimide, and P-chloromercuribenzoate, andby Cu, Hg, and Fe

Panaeolus β-fructo- Molecular weight — 1,16,000; most Mukherjee andpapillonaceus furanosidase active on sucrose; Ag and Hg are Sengupta

(inulinase) highly inhibitory, sucrose; inulinase (1987)= 5.7; optimum temperature = 60–65°C,and pH = 6.0; Fructose wasdetected as liberated sugar fromraffinose, stachyose, inulin

Pleurotus ostreatus Proline Extracted from mushrooms; Yoshimotoimino- optimum pH 7.2 and temperature 42°C et al.peptidase (1991)

KOH under N was developed; the results incomparison with the data in the literature led toa proposal that it is derived from a new Nprecursor (Harki et al., 1997). The truffle mela-nins both from peridium and gleba tissues ofthe freshly collected fruiting bodies of Tubermelanosporum are allomelanins, which appearto be formed by an intimate, noncovalent asso-ciation between polyphenolics (Angelis et al.,1996). A novel pyridine derivative was iso-lated from the mushroom Albatrellus confluens,which promoted melanin synthesis by B16melanoma cells (Kawagishi et al., 1996). Ba-sidiomycetes have been recognized as the mostecologically significant group of organismsresponsible for lignocellulose decomposition(Swift, 1982). Furthermore, several basidi-omycetes are known to have the ability to syn-thesize de novo organohalogen metabolites.Both chloromethane (Harper, 1985) and sev-eral types of chloroaromatic metabolites, suchas chlorinated anisyl metabolites (Hsu et al.,1971; Dominguez et al., 1972; Van Eijk, 1975;Takahashi et al., 1993) and chlorinated orcinolmetabolites (Okamoto et al., 1993) are producedby wood- and litter-degrading basidiomycetes.Species belonging to genera Hypholoma,Mycena, and Bjerkandera showed specific ad-

sorbable organic halogen (AOX) production,in the range of 1074–30, 893 mg kg–1 dry weightof mycelial biomass; these species were alsoable to produce AOX when cultivated on natu-ral lignocellulosic wastes (Verhagen et al.,1996). Metabolism underlying the productionof halogenated compounds by the white-rotfungus Bjerkandera adusta was studied directlyfrom the growth medium by membrane inletmass spectrometry and tandem mass spectrom-etry (Beck et al., 1996). The levels of biogenicamines (the basic amines that form a group ofantinutritional compounds, increased intake ofwhich can exert psychoactive and/or vasoac-tive effects) found in Agaricus bisporus andBoletus species were safe for human consump-tion (Kalac and Krizek, 1997).

Two novel azepine derivatives were iso-lated from the ethanol extracts of fruiting bod-ies of the pungent mushroom, Chalciporuspiperatus (Sterner et al., 1987). Three novelsesquiterpene ethers as natural products wereisolated from the liquid cultures of brown-rotfungus, Lentinus lepideus (Abraham et al.,1988). Three of the four steroids from Agaricusblazei were cytotoxic against Hela cells(Kawagishi et al., 1988). Yields of indole alka-loids viz., Psilocybin, Psilocin, and Baecocystin

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from Psilocybe, Panaeolus, Stropharia,Inocybe, and Pluteus were improved by theaddition of tryptamine to the growth medium(Gartz, 1988; Gartz, 1989a). Substituted in-doles (e.g., tryptamine) were manufactured insolid-phase fermentation by species ofPsilocybe, Panaeolus, Stropharia, Inocybe,Conocybe, and Pluteus (Gartz, 1989a,b). Anti-fungal diterpenic esters of 16-hydroxygeranyl-geraniol and mesaconic and/or fumaric acid(that prevented Cladosporium spore formation)were isolated from Boletus cavipes (Toyotaand Hostettmann, 1990).

Low acetylation degree chitosan was pro-duced in wheat straw cultures (SSF) (6.18 g kg–

1 of fermentation medium), which gave up to50 times yields of other chitosan productionmethods from fungi. This is proposed to pro-vide a new flexible and easily scaled up proce-dure for the production of such chitosan(Crestini et al., 1996). From 1 g of fruiting bodyof Lyophyllum cinerascens, proline endopepti-dase (3.1)2, dipeptidyl peptidase (0.48)2, andproline iminopeptidase (14.4)2 units per gramwere recovered (Yoshimoto et al., 1989).

About 75 species of white-rot and brown-rot fungi were examined for the production ofsecondary metabolites. Low nitrogen culturingof Lentinus lepideus produced p-methoxyphenylpropanol, a new secondary metabolite; incuba-tion of the culture with p-coumaric acid,p-methoxycinnamic acid, ferulic acid, isoferulicacid, and methyl-ferulate yielded a variety ofphenyl propanol derivatives. Only the brown-rot fungus, Daedalea dickinsii produced me-thyl p-methoxycinnamate (Ohta et al., 1990),4-hydroxymethyl quinoline was isolated fromPolyporus versicolor and Polyporus sanguineus(Abraham and Spasov, 1991). Repandiol, a newdiepoxide isolated from Hydnum rependum,displayed potent cytotoxic activity against vari-ous tumor cells (Takahashi et al., 1992).

Diterpenoid acids possessing the abletaneand pimarane skeletons isolated from Armillariamellea in liquid culture known collectively asresin acids have not been reported previously. Inaddition, dehydroabietic acid, pimaric acid,isopimaric acid, and sandaracopimaric acid,

levopimaric acid, endo-peroxide, 7-oxodehydro-abietic acid and 7-oxo-15-hydroxydehydroabieticacid were obtained (Ayer and Macaulay, 1987).Ursocholic acid was produced by in vitro cultur-ing of Polyporus, Coriolus, Daedaleopsis,Paneolus, Marasmius, Crinipellis, and Pholiota(Terada et al., 1986b).

Riboflavin was identified as the light emit-ter from the gills (Uyakul et al., 1990) inLampteromyces bioluminescence (Isobe et al.,1987); the structure was assigned as pento-furanosyl riboflavin (Isobe et al., 1988; Deonand Schwartz, 1988). Its synthesis was studied(Isobe et al., 1987, 1989). Lampteroflavin ex-tracted from Lampteromyces japonicus may beused as a UV absorber in cosmetics (Isobe andGoto, 1988).

Chemical investigation of pest/insectcontrol agents produced by mushrooms ledto the isolation of clitocine, a new nucleo-side from Clitocybe inversa. It showed stronginsecticidal activity against the pink boll-worm Pectinophora gossypiella (Kubo et al.,1986). An antiallergy agent coustin (a gly-coprotein) was extracted from the mush-room, Sorcodon aspratus (Fujimoto et al.,1988).

Polyporus is reported for its ability to pro-duce benzaldehyde and benzoic acid (Kawabeand Morita, 1994) (Figure 6). Coprinolone, anoxygen-bridged protoilludance from Coprinuspsychromorbiolus, was formed (Starratt et al.,1987). Neogrifolin and grifolin obtained fromthe lipophilic fraction of methanol extracts ofPolyporus confluens showed inhibition of rootgrowth of Chinese cabbage seedlings (at 50and 100 ppm, respectively). Grifolin (2-trans,trans-farensyl-1-5-methyl resorcinol) andneogrifolin (4-trans, trans-farensyl-5-methylresorcinol) were identified as the plasma cho-lesterol-lowering components from Polyporusconfluens (Sugiyama et al., 1992). Vanillyl al-cohol and veratryl alcohol were added to aculture of Tyromyces palustris or Coriolus ver-sicolor, in which the culture medium containedglucose and cellobiose, to produce vanillyl-D-glucoside or veratryl-D-glucoside (Kondo et al.,1988).

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FIGURE 6. Proposed production pathway of benzaldehyde and benzyl alcohol by Polyporus tuberaster. (Adaptedfrom Kawabe and Morita, 1994.)

All aerobes are at risk of being damaged byactivated oxygen species such as superoxideradical, hydrogen peroxide, hydroxyl radical,and singlet oxygen (Endo and Asada, 1992), astheir high reactivity often results in injury, in-cluding carcinogenesis, inflammation, and ag-ing (Oyazagui, 1980). In biological systems,however, antioxidant enzymes such as super-oxide dismutase (SOD) (Fridovich, 1975), glu-tathione peroxidase, and catalase (Fridovich,1976) have a protective role against oxygentoxicity. As an enzyme that catalyzes the con-version of superoxide anions into normal oxy-gen and hydrogen peroxide, there are manyreports on the trial of SOD to treat variousdiseases concerned with superoxide (Niwa,1992a). However, the therapy must be done byinjection, because SOD is inactivated by diges-tive enzymes and gastric juices when it is orallyadministered. An alternative approach in thefield of food is to find low-molecular-weightcompounds that mimic SOD activity (Niwa,1992b) or which can enhance the activity ofSOD. In this context, Kim et al. (1994) have

screened SOD-like compounds and activatorsof SOD in the extracts of mushrooms (Table 27)fruits and vegetables by measuring their effectson pyrogallol auto-oxidation, which is cata-lyzed by superoxide anion. Such activators maybe very important in biological systems be-cause erythrocytes in blood are continuouslyexposed to superoxide anion generated by theauto-oxidation of hemoglobin (Misra andFridovich, 1972). After identification andcharacterization, SOD-like compounds and ac-tivators of SOD could be used to formulatehealth foods, because they are superior to theenzyme in the aspects of duration, time, admin-istration method, production time, and adverseeffects.

VI. BIOLOGICAL ODDITIES

Mushroom species with their tremendouspotentialities to biosynthesize a highly variablerange of enzyme systems catalyze accordinglya range of useful synthetic and degradativereactions. These in turn have led to a number of

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TABLE 27Superoxide Dismutase (SOD)-Like Activity ofAqueous Extracts of Mushrooms, Fruits, andVegetables

Species SOD-like activity a

Nameko (Flammulina velutipes) 41Garlic (Allium sativam) 40Oriental lettuce (Lactuca sativa) 36Strawberry (Fragaria species) 32Oyster mushroom (Pleurotus ostreatus) 30Onion (Allium cepa) 30Shiitake (Lentinus edodes) 28Spinach (Spinacea oleracea) 20Grape fruit (Citrus paradisi) 19Cabbage (Brassica oleracea) 14Carrot (Daucus carota) 14

a SOD-like activity (%) = (A–B) × 100/A.

Note: Where A and B are the autoxidation rate of pyrogallolin the absence and presence of plant/mushroom ex-tracts, respectively.

Adapted from Kim et al., 1994.

biological useful derivations/oddities, which arereviewed below.

The subject of bioluminescence of mush-rooms is discussed with 10 references. In thechemiluminescent moon light mushroomLampteromyces japonicus, extraction, purifi-cation, and structural elucidation of lamptero-flavin were conducted (Isobe and Goto, 1990).The luminescence of the CO adduct of twoisoenzymic tyrosinases isolated from Agaricusbisporus (Kanagy et al., 1988), and also radio-activity in fresh mushrooms (Fromm, 1989)are delineated.

From wood chips, by incubation of the chipswith Pleurotus ostreatus (beech), Coniophoraputeana (pine) and Fomitopsis pinicola (spruce)fibre board was produced. Wood fiber struc-tures, e.g., fiber board, were manufactured bydefibering wood chips, inoculating the fiberswith a pure culture of Trametes versicolor in-ducing white-rot and fermenting for approxi-mately 7 days (Wagenfuehr et al., 1989a,b).

Total digestible nitrogen contents ofsteamed and crushed remnants of Japanese oaklogs (that had been used for culturing of Lentinusedodes) were 41.3 and 15.8%, respectively,

which were available for both beef cows andfattening steers as roughage sources, if the short-ages of crude protein and minerals were rem-edied by supplementation (Otsuki et al., 1991).Boiled cereal grain and soyabean meal fer-mented with Pleurotus ostreatus and Pleurotusflorida at pH 5, and 60 to 70% humidity provedto be a high protein feed when fed to swine,who then showed higher weight gain (Mileaet al., 1988). Spent rice straw substrate afterculturing of Pleurotus was found non-toxic (Zakia Bano et al., 1986) and in its biode-graded form has advantage to serve as an up-graded ruminant feed (Rajarathnam and ZakiaBano, 1978b; Zakia Bano and Rajarathnam,1989).

The products obtained by pyrolytic carbon-ization of waste mushroom culture beds, fol-lowed by inoculated growth of bacterium, Ba-cillus subtilis, are useful as soil improvers,fertilizers, preservatives, and feed (Tan, 1992).Spent mushroom substrate can be diverted forproduction of granulated organic-mineralfertilizer after suitable supplements with lig-nin, salts, and manure PO4 followed by granu-lation (Szmidt et al., 1992).

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Spent residue, after growing Pleurotussajor-caju on Ricinus communis and Morusalba, was able to enhance biogas production,besides producing a high percent of methane,compared with the undegraded wastes (Sharmaet al., 1989). The biogas production from theanaerobic digestion of rice straw with Pleurotusflorida was 8-fold more than from the unde-graded straw (Mehta et al., 1990). Mycostrawstreated with Pleurotus sajor-caju resulted inincreases in biogas production over the un-treated lots, which varied from 21.5% withspent bagasse to 38.8% with spent rice straw(Bisaria et al., 1990).

A biofilter made of plant material inocu-lated with white-rot species of Polyporus,Stereum, Marasmius, Pleurotus, and Sporotri-chum could decontaminate waste gases, odors,aromatic compounds halohydrocarbons, andvolatile inorganics (Huettermann et al., 1989).An air filter prepared by loading a porous inor-ganic support (Zeolite or activated carbon), witha slurry containing the powder of dried mush-room such as Agaricus bisporus or Agaricusxanthoderma, could remove 62% tar, nicotine,and 3,4-benopyrene from the cigarette smoke(Kondo and Kondo, 1987).

Mushroom-origin oridases and oxidizedplant polyphenols are thought to be oxygendonors and to decrease the volatility of fecalodor, and oligosaccharides and dietary fiber toimprove in intestinal conditions for lactic acidfermentation by enteric bacteria (Tanaka et al.,1992).

Mushroom powder was used as a modelsystem to study the extraction of oleoresinswith supercritical CO2 (Del Valle and Aguilera,1989). Microscopic scan and X-ray analysisrevealed the presence of clusters of calciumoxalate crystals (as fruiting body drugs) withelements such as Si, Al, K, and P in species ofPolyporus, Poria, Russula, Fomitopsis andGanoderma (Tanaka, 1990). Medium, rich incalcium sulfate, tended to produce calcium-high Lentinus edodes (Sasaki, 1990). Mutabil-ity and abnormal development of the life cyclewere responsible for self-fructification in

Coprinus radiatus (Ozier-Kalogeropoulos andGuilaemet, 1989).

Sago hampas, the fibrous pith residue leftafter starch extraction from sago palm, is abun-dant at sago-processing factories and can beused as a substrate for the production of laccaseby solid substrate fermentation (SSF) withPleurotus sajor-caju, an edible mushroom. Themaximum laccase activity could almost bedoubled after 6 days of fermentation by addi-tion of 0.2 mM vanillin or ferulic acid; thecellulose to lignin ratio increased significantlyduring the 12 days of SSF, from 2.74 in thecontrol to 3.3, when 0.2 mM of either vanillinor ferulic acid was added to the substrate(Kumaran et al., 1997). Apple juice was clari-fied and stabilized by enzymic oxidation withpolyphenol oxidase (laccase) from Trametesversicolor combined with cross-flow ultra-filteration on a pilot plant scale (200 L) (Maieret al., 1990). Fibrous wastes such as wool cut-tings, rabbit fur, and pig bristles were disposed(as useful feed or fertilizer) by using extracel-lular enzymes produced by Pleurotus ostreatus(Jonas and Schanel, 1990). The extraction ofmushroom tissues for the production of phenol-oxidase is a simple method for utilization inenvironmental protection services (Steffen etal., 1995).

Mushroom flavor was prepared containing1-oceton–3-ol as a main ingredient from thecultured extract of Coriolus versicolor; the fla-vor was then prepared as an inclusion com-pound in cyclodextrins (Sato et al., 1991).Shiitake was used in the preparation of instantfoods, along with carbohydrates, cabbage, beansprouts and cuttle fish (Ichikawa, 1991).Polypore species and herb (ex. sage) weresoaked in vinegar to give an extract for use asa health drink (Numata, 1988). A fermentedmilk product rich in nutrients and potassiumwas prepared from low-fat milk and Lentinusedodes (Kanetani, 1990). In an analysis of tasteof mushrooms, among the 5-nucleotides, 51-CMP and 51-AMP were present at greater lev-els than 51-UMP and 51-XMP. Among freeamino acids, total MSG-like amino acids

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(Glutamine +Aspargine) were in the majority.The synergistic effect of glutamine and 51-GMPfor MSG was higher in the cap than in stipe(Tsai and Tsai, 1987).

Lentinus edodes was used as a source ofpolyphenol oxidases to treat mono or diphenols,to produce pigments, for use in preparations ofhair dyes (Saruno, 1991). Mushroom extractswith melanin precursors were useful in prepa-ration of hair dyes (Kanetaka and Myata, 1991).

A cosmetic containing polysaccharidesextracted from Lentinus edodes was used asskin or hair conditioner (Shiraishi and Hayashi,1991). Water containing humic acid was con-tacted with species of Pleurotus or Coriolus,under aerobic conditions to decompose humicacid; its removal reached 80 to 90%, comparedwith 20 to 30% by the conventional coagula-tion method (Sugata 1989a,b).

VII. CONCLUSIONS

Thus, in lacking chlorophyll, mushroomsrepresent a very distinct group of organisms,their biological systems being very unique,compared with other plant systems. They de-pend on inedible plant materials for their nutri-tion and growth. They have the unique abilityto biodegrade these wastes and return the car-bon to the atmosphere as CO2 in its most natu-ral form; the significance of their role is em-phasized, when one learns that CO2 accountsfor only 0.04% of the atmosphere and any slightincrease would destroy the balance of millionsof organisms living on Earth. It is estimatedthat each year 1 acre of forest land is coveredby nearly 2 tons of debris. Without these fungi,the decomposers, to do the clean-up job, ourtrees would be buried in no time by their cast-off leaves and branches (Booth and Harold,1982). It is also amazing to learn that some ofthem are known to have a role in fixing theatmospheric CO2. Further, their higher yield,approximately five times that of cereals likerice per unit land and their protein conversion

efficiency, approximately twenty times that ofmeat generating animals (Rajarathnam andZakia Bano, 1991; Rajarathnam et al., 1992),makes these organisms a set of microbes un-paralleled with any other organism on ourplanet. The most glorious point is their abilityto bioconvert and biotransform the inediblewastes directly into palatable forms of food,leaving behind a substrate that commends thevalue of a number of diversified useful applica-tions and implications. While higher plants aregrown for their edible part in the form of grains,oil seeds, pulses, fruits, vegetables, and so on,these fungi strike the other side of the coin andturn the inedible plant residues (left after theharvest of edible portions) into valid forms offood. Further, their essential amino acids, un-saturated fatty acids, good quality protein, car-bohydrates of non-starchy nature, valued di-etary fiber vitamins of B-complex, folic acid,potassium, phosphorus, and available iron, ad-vocate for the impartial placement of thesemicrobes in the position of foods of distinctnutritional value (Crisan and Sands, 1978; ZakiaBano and Rajarathnam, 1988; 1994; Zakia Banoet al., 1992; Chang et al., 1993). Theirhypocholesterolemic, hypolipidemic, anti-tu-morous, antibacterial, antiviral activities, in-cluding references on an anti-AID viral prop-erty, contribute to their medicinal virtues ofdistinct rank. Looking at these points, it is ob-vious that these mushrooms serve to be thenatural biological agents to resort to for diver-sification of plant wastes into merited ways ofdisposal. In view of the rigorous enactment oflaws targeted to prevent atmospheric pollutiondue to burning of plant residues, employingthese useful fungi can serve to avert atmo-spheric pollution (Wood, 1986; Penn, 1976;Hayes and Lim, 1979). Fruiting bodies of mush-rooms were considered ideal for the purpose ofevaluation as biosorbents, because it has beendemonstrated that many species exhibited highbiosorptive potentials (Muraleedharan et al.,1995). These fungi display unique biologicalcharacteristics to decompose several of the

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pesticides, and recalcitrant organic compoundscausing atmospheric pollution (Paszcznski andCrawford, 1995).

Their capacity to biodegrade lignin is amajor task that cannot be equated with anyother biological agents. As it is well docu-mented, lignin is the most resistant form ofplant product of photosynthesis, in nature, andaccounts for 25 to 50% of the plant biomassgenerated. While physical methods to break-down lignin require a lot of energy, chemicalmeans lead to undesirable pollution of the sur-roundings (Rajarathnam and Zakia Bano, 1989,1991). The barrier is to use up the cellulo-hemicellulosics most actively, as lignin is bro-ken down by several of the white-rot mush-rooms, thus they occupy a pivotary role inlignin degradation. Several of the white-rot species are potential agents to secreteand produce a number of oxidative enzymesinvolved in lignin biodegradation. Their roleis vital and significant in mineralization of lig-nin. Conditions promoting their productionwhile culturing, conditions favoring their sta-bility and conditions optimum for metabolicactivities of several species and strains, obvi-ously would require an unretiring research ef-fort. Ultimately, this would aid in gaining moreinsight into the degradation of the most com-plicated phytogenic compound on earth, i.e.,lignin. There is tremendous potential in em-ploying these enzymes/enzyme producers, fora number of applications of lignocellulosicssuch as pulping, bleaching, waste water treat-ment, conversion of lignin into useful productsand so on.

They secrete a number of enzymes to de-grade cellulose, hemicellulose, lignin, pheno-lics, proteins, and so on, which has rendered itpossible for them to thrive over a large spec-trum of inedible plant wastes. Further, the de-graded products released are transformed intoseveral unique mushroom constituents bearinga role in their nutritional/medicinal value. Thus,these mushrooms have multitudinal enzymesystems to biosynthesize and design their own

cellulose, chitin, protein, amino acids, unsatur-ated fatty acids, flavor constituents, texture,structure, color, etc. At this juncture, to decidewhether their capacities and capabilities to “bio-degrade” (Figure 7A) are superior to “bio-synthesise” (Figure 7B) is highly debatable.Research efforts worldwide are pouring in, yearby year, they pile up and substantiate theiradditional useful properties of biodegradationand biosynthesis. What might be interesting isto draw several correlations with at least a fewof the species, between these two properties,on several of the growth substrates, under con-trolled conditions. This would aid in drawingthe most useful data, on how the biologicalsystems are operating and functioning, for theformation of the mushroom “fruiting body”,which is the net result of catabolic and anabolicfunctions of the mushrooms. This draws us tothe ultimate consideration of the cellular me-tabolism required to generate mycelium coupledwith induction of fruiting primordia, followedby growth into mature mushrooms. The mostprobable answer lies in looking into the func-tioning of ultrastructural components of thecells, at various levels of organisation, that havea direct influence on their morphogenesis. Ofcourse, it is essential to remember that there isa great degree of genetic diversity due to theirhaploid genetic constitution, rendered more firmby the dikaryotic state — a stage via media anda step on the way to the diploid phase of higherorganisms. The production of basidiosporeswith segregation and aggregation of nuclearcomponents involving higher rate of variabilitydue to genetic incompatability of multiple alle-les — tetrapolar inheritance and so on, hasresulted in evoking the highest chances of vari-ability amongst the mushrooms (Chang et al.,1993). What appears to be a requirement byman is to trace the pathways of generation ofthese desired variations and means and meth-ods to protect them and render them stable.This may perhaps be the most efficient way ofexploiting the mushrooms for further usefulfunctions.

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ACKNOWLEDGMENT

The authors gratefully acknowledge the fi-nancial support of the “Mushroom Project”, bythe Department of Biotechnology, New Delhi,India.

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biodegradative and biosynthetic capacities of mushrooms: present and future strategies

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