Soil Microbiology—It's a Small World1

FRANCIS E. CLARK2

ABSTRACT would run high risk of being numbered with the deceasedSoil Microbiology-It's a Small World. ere l COuld reacllthe door' ' .

The science of microbiology owes much of its origin toThe accomplishments and personalities of some notable early Amer- arguments about spontaneous generation. Soil microbiol-

ican soil microbiologists are discussed. The tangled skeins of influences ogists> however, do not spring forth by spontaneous genera-and interactions among them are used to justify the small world con- ^ n± thdr appearance is the result both of their owncept used in the title In discussing the subject matter of soil microbiol- indinations or genetic makeup and of the environment toogy, it is noted that as society becomes more concerned with popula- . - i_ L. j r - .A • - i • u - iUon growth and world food supply, energy sources and requirements, which they are exposed. For early American soil microbiol-and ecology and the environment, soil microbiology is shifting its em- °gists, the environmental influence was often tenuous andphasis from soil and the growing plant to man and the biosphere. The circuitous, but if one delves into biographies, he cannotsoil microbiologist is becoming increasingly involved in exposing such help but be impressed by the tangled skeins of influencesunesthetic substrates as sewage, animal manures, and food and fiber among individuals, whether they were in the same labora-processing and sanitary landfill organic wastes to microbial attacks. tory or whole continents apart. These tangled skeins prac-His objectives are to make such substrates less objectionable environ- tically demanded use of the title—''Soil microbiology, it'Smentally and to exploit their residual food and energy potentials. „ small world "Together with these endeavors he is expanding his efforts to define the There can ^ ̂ doubt buj ̂ Qur first American soj,dominant roles of microorganisms in the functions of terrestrial eco- . . . . . . ., , , , , . ,systems. Therein, microorganisms metabolize a far larger amount of microbiologists were influenced by notable pioneers else-the net primary productivity than do all of the higher forms of life, where—Wmogradsky and Omehanski in Russia, Hiltnerinclusive of man, taken collectively. and Lbhnis in Germany, Beijerinck in the Netherlands, and

Russell in the United Kingdom. There possibly can be_________________ argument as to just whom first should be named as a notable

American soil microbiologist. Inasmuch as I have to start

IN THIS BICENTENNIAL YEAR, the nation as a whole has somewhere, I am going to conform to widely held con-been expending considerable effort in looking back at sensus and name Jacob G. Lipman. To any dissenters, I

where it has been and forward to where it is going. In defer- readily admit that Jacob Lipman took his doctoral degree inence to the celebration, your Society officers suggested that biochemistry, and not in soil microbiology, and that heto the extent practical each division schedule at least one spent most of his professional career not in soil microbiol-presentation with a bicentennial flavor. Presumably they ogy but as the director of the New Jersey Agricultural Ex-meant something nostalgic but strictly noncommercial, lest periment Station. Among his numerous achievements heit jeopardize the tax-exempt status of the Society. Accord- served as the president of the First International Congress ofingly, I will not attempt to sell you any handpainted red, Soil Science and he founded the well-known periodical,white, and blue bacteria. I will attempt firstly to call atten- Soil Science, in itself a continuing memorial to him.tion to some notable early American soil microbiologists Lipman recognized that the soil was a complex and livingand, secondly, to take some note of the current status of the entity and that soil microbiology was an integral part of soilsubject matter of soil microbiology. science. He was interested in soil microbiology as it related

In my discussion of pioneer soil microbiologists, I shall to soil fertility and crop production. His students and co-consider almost without exception individuals born before workers carried this philosophy to other institutions. One1900. Many of whom I shall speak are deceased. Of those such was P. E. Brown who, as a departmental head at Iowanow living, probably none is in the audience. Con- State University, fostered a strong interest in soil microbiol-sequently, disproportionate attention given to some individ- Ogy as it related to soil fertility. Among soil microbiologistsuals at the expense of their equally notable contemporaries taking work at Iowa State and qualifying for mention hereshould largely go unchallenged. Were I to undertake evalu- because they were born before 1900 are the following: F. E.ation and discussion of the contributions of the many soil Allison, W. B. Bollen, L. W. Erdman, F. B. Smith, and S.microbiologists born since 1900 and currently present, I c. Vandecaveye.

v- Inasmuch as I have mentioned P. E. Brown (who left^ ~T~ • f A D c t ic i^A c ,. ^ ir ^ i D- - i Rutgers to establish a program at Iowa State) I most cer-Conlnbution from ARS-USDA, Fort Colhns, Colo. Bicentennial " , ,

address presented before Div. S-3, Soil Science Society of America, 29 tainly must mention two of Lipman S colleagues who bul-Nov. 1976, in Houston, Texas. Received 30 Aug. 1976. Approved 5 Nov. warked the soil microbiology program at Rutgers after Lip-' "^Formerly Microbiologist, now Collaborator, USDA-ARS, P. O. Box man became involved in administration and after his death.E, Ft. Collins, CO 80521. These two were Selman A. Waksman and Robert L. Star-

CLARK: SOIL MICROBIOLOGY 239

key. Waksman's Principles of Soil Microbiology and Waks-man's and Starkey's The Soil and the Microbe were thestandard reference and teaching texts for soil microbiologyduring the second quarter of this century.

In the latter part of his career, Waksman received world-wide recognition because of his role in the discovery ofstreptomycin and his reception of the 1952 Nobel Prize inPhysiology and Medicine. As a part of the streptomycinfallout, he received many honorary doctorates from foreignand domestic universities. Many years earlier, in 1918 to beexact, Selman Waksman obtained his earned doctoral de-gree at the University of California, Berkeley. A juniormember of the examining committee was Ivan C. Hall. At alater date, Dr. Hall was my major professor at the Univer-sity of Colorado. After Dr. Waksman's death in 1973,much of his personal library was given to the American So-ciety of Microbiology for distribution as it saw fit. Severalvolumes went to Ivan Hall, who was then nearing his 90thbirthday, and Hall immediately offered those volumes tome. Indeed, it is a small world.

Development of soil microbiology at the University ofWisconsin was principally fostered by Edwin B. Fred. Dr.Fred obtained his doctorate in Germany in 1911 and joinedthe University of Wisconsin faculty in 1912. He served thatinstitution for 46 years, the last 13 as president. Dr. Fred,together with coworkers Ira L. Baldwin and ElizabethMcCoy, established a legume microbiology program atWisconsin that became internationally acclaimed. Doubt-less some of you here present have read, either voluntarilyor by assignment, classroom material prepared by Dr. Fred.In 1916, he published a Laboratory Manual of Soil Bacteri-ology, and in 1928 and joint with Waksman, a second man-ual entitled A Laboratory Manual of General Microbiology,with Special Reference to the Microorganisms of the Soil.Jointly with Felix Lbhnis, he published A Textbook of Agri-cultural Bacteriology.

In speaking of the soil microbiology program in the U.S.Department of Agriculture, I especially wish to mentiontwo individuals, Felix Lbhnis and Charles Thorn. The firstof these possibly should not be named as an American mi-crobiologist inasmuch as he made his reputation as a soilmicrobiologist in Germany before joining the USDA in1913 and in 1923 he left the department to return to teachingin Germany. Lbhnis became widely known largely becauseof his several books. His manual of methods, Land-wirtschaftlich-bakteriologisches Praktikum, was translatedinto English, French, Polish, Russian, and Japanese. HisHandbuck der landwirtschaftlichen Bakteriologie, togetherwith his Einfiirhrung in die Bakteriologie and Vorlesungenuber landwirtschaftliche Bakteriologie, were the standardsoil microbiology texts or references during the first quarterof the 20th century, just as Waksman's and Starkey's bookswere the standard references in the following quarter cen-tury. In the United States, Lohnis collaborated with Dr.Fred, as just mentioned, to publish a Textbook of Agricul-tural Bacteriology and with Nathan R. Smith to author LifeCycles of the Bacteria. At the time of Lohnis' death in1930, Nathan Smith wrote of him: "He was very intolerantof work poorly done, of old facts published as new, or ofover-emphasis as to the importance of the work, and he didnot hesitate to express himself in very choice language."

Charles Thorn joined the USDA in 1904 and served aschief of the Microbiological Laboratory in the Bureau ofChemistry from 1913 to 1927 and as head of the Division ofSoil Microbiology from 1927 and 1942. One member of thedivision was N. R. Smith, who entered the USDA in 1911.Thorn's major books included: The Aspergilli in 1926 withMargaret Church; The Penicillia in 1930; and Manual of theAspergilli in 1945 and Manual of the Penicillia in 1949,both with K. B. Raper. Thorn was also quite prolific in giv-ing presidential addresses. During his career he served aspresident of the Mycological Society of America, the Amer-ican Society of Microbiology, the Society of Industrial Mi-crobiology, the Bacteriological Society of Washington, theBotanical Society of Washington, and the WashingtonAcademy of Sciences. In his presidential addresses, he usedsuch titles as "The Colony," "A Microbiologist Digs in theSoil," and "Out of the Furrow."

Prior to this meeting, your program chairman asked me toinclude in this discussion some of my personal experienceswith early American soil microbiologists. Except for one in-cident, I must forego such narrations simply because of thetime factor. Dr. Wagner, in making his request, doubtlessknew that I had had contact with nearly everyone of whom Ihave spoken. I must confess that I never knew Felix Lbhnis,but when in France in the 1940's, I did call on SergeiWinogradsky, who was born in the year 1856.

The one incident that I am going to recall concernsCharles Thorn, the man who was always in a hurry. Hecame to work early in the morning. At national meetings heusually could be found at an early hour standing outside thecoffee shop waiting for the doors to open. One August inthe late 1930's, after Thorn and myself had spent 3 days inthe cotton fields in the Gila and Salt River valleys in Ari-zona, with midday temperatures as high as 46°C (115°F),we boarded a night train in Phoenix for travel to Riverside.At least some of you present may recall that the great tide ofair travel did not come until after the 1930's. In Riverside,Thorn and I were to detrain at 5:00 am, and wait in the sta-tion until about 7:00 am for Salinity Laboratory scientists toarrive and take us to breakfast, and thereafter to the Labora-tory. At 5:00 am, I dragged myself to the train vestibule,and there stood Charles Thorn. The instant the train stoppedhe jumped down and started walking just as fast as he couldin order to traverse the 50 m to the station where we were towait about 2 hours. This was the last straw, so by virtue ofmy longer legs and early morning ill humor, I managed towalk right past Thorn, almost as if he were standing still. AsI was about three steps ahead, a querulous voice came fromover my shoulder: "Please tell them that I'll be thereshortly."

Finally, I wish to name A. G. Lchhead, a Canadian na-tional who neither worked nor studied in the United States,as a notable early American soil microbiologist. In 1912,Grant Lochhead went to Leipzig to study soil microbiologyunder the tutelage of Felix Lbhnis. He had not completedhis doctorate at the time of the outbreak of World War I,and, as an alien national, he was detained in Germany untilafter the close of that war. The detention camp to which hewas assigned had formerly been a race track, and the habita-tions for the prisoners were they haylofts and the horsestalls.

240 SOIL SCI. SOC. AM. J . , VOL. 41, 1977

In 1929, Dr. Lochhead was appointed Head of the Bacte-riology Division of the Canada Department of Agriculture.Lochhead established a varied and productive program thatI shall not attempt to discuss in detail, but I do recommendhis History of the Bacteriology Division of the CanadaDepartment of Agriculture 1923-1955. Two of Lochhead'sstaff who became well known were M. I. Timonin and H.Katznelson. Both were Russian-born and both chose to taketheir doctoral work at Rutgers, a choice possibly due at leastin part to the fact that Lipman and Waksman were also Rus-sian-born. Others of Lochhead's staff came from the Uni-versity of Wisconsin, and as already mentioned, Lochheadhimself studied with Lbhnis. Our small world concept ofearly American soil microbiology overlaps national bounda-ries.

The time factor does not permit me to discuss other earlyAmerican soil microbiologists born before 1900. Namesthat have not thus far been mentioned even fleetingly, andthat come quickly to mind because I knew the individualspersonally, are those of P. L. Gainey in Kansas, J. E.Greaves and T. L. Martin in Utah, I. M. Lewis in Texas,and in New York, J. K. Wilson at Cornell and H. J. Conn atGeneva. I am sure that as a group, the present audiencecould greatly extend this listing.

Now let me turn my discussion from the founding fathersand focus instead on the subject matter of soil microbiol-ogy. As a point of departure, I am using the invitationalpaper presented to this Division by Frank Allison on the oc-casion of the 1961 Silver Jubiliee of this Society (Allison,F. E. 1961. Twenty-five years of soil microbiology and alook to the future. Soil Sci. Soc. Am. Proc. 25:432^39.).In that paper, Allison discussed the subject matter of soilmicrobiology under eleven headings. These were: soil pop-ulation, organic matter, nutrient availability, symbiotic andnonsymbiotic nitrogen fixation, nitrogen losses, soil ag-gregation, antibiotics, pesticides, rhizosphere, and biologi-cal control. If one reads Allison's paper in its entirety, hefinds that the emphasis is largely on the direct role of micro-organisms in soil science. Allison stated that there are fewphases of soil science in its fundamental or applied aspectswhere microorganisms do not play a major role. This gener-al theme was also that of Lipman, Lohnis and Fred, andeven of Winogradsky—"On pourra parler de microbiol-ogie agricole comme d'une science constitute, dont I' im-portance pour V agriculture ne saura etre estimee assezhaul." Lipman's initial assignment in soil bacteriology wascouched in more mundane terms—''. . . t o investigate themovement of plant-food in the soil, and the part of bacteriain the formation, changes, or destruction of such plant-food."

To determine whether or not soil microbiology has aban-doned its traditional study areas in the 15 years interveningbetween Allison's presentation and this bicentennial year, Iclassified under Allison's subject matter headings all Divi-sion S-3 papers in the SSSA Proceedings for the 3 years pre-ceding both the 1961 jubilee year and this bicentennial year.During each period, nitrogen transformations and organicmatter characterizations or decompositions accounted forroughly two-thirds of all the papers published. There wassome evidence of a shift of interest from soil aggregation(the papers thereon dropped from 13% to 2%) to pesticide

studies (these increased from 4% to 15%). In both periods,population and growth studies accounted for roughly 9%,and studies on the rhizosphere, antibiotics, and biologicalcontrol individually constituted 4% or less of the publica-tions. However, although there is evidence that soil micro-biology has not abandoned its former areas of interest, it isnonetheless true that studies within these areas, particularlythose dealing with nitrogen and organic matter, have as-sumed a quite different bias.

Formerly, studies on nitrogen losses were concerned withthe efficiency of recovery of soil or fertilizer nitrogen by thegrowing plant. Nitrogen not recovered in the crop wasviewed primarily as an economic loss. Current concern iswith what happens to the soil or fertilizer nitrogen that is notused by the vegetation. Does such nitrogen leach to causehigh nitrate content in groundwaters, or is it washed intosurface waters to cause unwanted eutrophication? Deni-trification, viewed in the past as a highway robber, is undersome circumstances now viewed as a good Samaritan for itsconversion of nitrate nitrogen to atmospheric nitrogen, butstill as a villain in its production of nitrous oxide.

In the past, studies on organic matter were commonlyconcerned either with the effects of its decomposition onsoil tilth or on the tie-up and release of essential plant nu-trients. Attention was given primarily to the natural litters ofthe field and forest. Microbial digestion of municipal sew-age had long been employed, but this was in the domain ofthe sanitary engineer and hardly concerned the soil microbi-ologist. Recalcitrant organic sewage was taken from thedigestion tanks and then dried and burned. With the imposi-tion of clean air requirements, burning of sewage sludgewas no longer permissable, and the soil microbiologist sud-denly found himself confronted with the problem of howmuch sewage sludge could be tolerated on agriculturallands. Likewise, the rates of loading and the timing sched-ule for making land distributions of the organic wastes fromlarge-scale food and fiber processing operations became im-portant questions. Because of clean water requirements,such wastes, as well as the manures from livestock feedlotssituated near streams could no longer be flushed directlyinto those streams.

In his current commitment to organic matter research, thesoil microbiologist is concerned not only with microbial in-cinerations and the maintenance of clean air and water butalso with what can be salvaged from organic wastes to meetthe food and energy requirements of a rapidly expandingpopulation. Heretofore, the use of microorganisms as a foodsource has been focused most commonly on the tank cultureof algae in mineral nutrient solutions. Today the soil micro-biologist is involved in studies on the conversion of organicwastes into single cell protein, or SCP. At this point in time,the SCP is being harvested largely for animal rather than forhuman food, but inasmuch as the malnutrition crisis in theworld is largely that of a protein shortage, the prospect ofgrowing microbes on energy-rich waste organics to provideprotein for human consumption is currently receiving inten-sive scrutiny. A closely related area of research is that of bi-ological nitrogen fixation. It is in this area that the soil mi-crobiologist has received general acclaim for hisaccomplishments. In the past, the student of nitrogen fixa-tion has operated largely as a self-contained unit. Almost

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single-handedly he isolated rhizobial strains and tested theireffectiveness on host legumes and their ability to competewith less effective rhizobia already present in the soil.Today the soil microbiologist is faced with the need formuch greater breakthroughs in biological nitrogen fixationand in these endeavors he needs the cooperation of plantgeneticists, plant physiologists, microbial geneticists, andmolecular biologists.

In brief, the growing involvement of soil microbiologistsin problems of air and water pollution and in methane andSCP production and in biological nitrogen fixation is pro-viding today's soil microbiologists with exposure toworkers in other disciplines. Conversely, these otherworkers are now looking to the soil microbiologist for helpin solving problems with which they too are deeply con-cerned.

This double exposure has been especially striking in stud-ies devoted to the analysis of terrestrial ecosystems. Suchstudies have emphasized the extent to which the very smallforms of life dominate the flow of energy in the biosphere.Let me touch briefly on this point. We can generalize thatthe green plants in a terrestrial ecosystem usually ac-complish a net dry matter production of about 1 kg/m2/yr,the equivalent of about 5,000 kcal of energy. Who are theconsumers of this energy? All the nonmicroscopic membersof the ecosystem metabolize something like 5% of the total,and the microbes, the remainder. That may sound incredi-ble, but if so, only because heretofore there has not beengeneral recognition of the large amount of microbial bio-mass. Of all the secondary producers, the microbes areoverwhelmingly dominant in biomass. Their dry weight in agrassland is of the order of 100 g/m2 to a soil depth of 30cm, a value that greatly exceeds that of all the large mam-mals, rabbits, mice, toads, snakes, gophers, birds, grass-hoppers, spiders and other invertebrates too numerous tomention. The dry weight biomass of large mammals on amanaged grassland varies from 1 to 5 g/m2, depending onthe stocking rate. The biomass of the small vertebratestotals no more than 2 g/m2 and that of miscellaneous inver-tebrates, likewise no more than 2 g/m2. In some measure-ments, microbes can even outrank the vegetation itself. In amanuscript recently prepared jointly with two coworkers,we have pointed out that in a grassland the phosphorus con-tent, in g/m2, of the microbial component is twice that of thevegetation. Furthermore, the cumulative uptake of phos-phorus by microorganisms during the growing season is five

times the seasonal plant uptake. This multiple is a reflectionof the higher metabolic and turnover rates of the microbialpopulation.

Quantification of the microbial phosphorus cycle has rev-olutionized simulation modelling of phosphorus flows interrrestrial ecosystems. Likewise, delineation of the dynam-ics of microbial nitrogen in the ecosystem has greatlychanged our concept of the nitrogen cycle. Heretofore, thestandard textbook concept has been that of available soil ni-trogen moving in turn to live vegetation, litter, and the soilorganic matter, followed by replenishment of the availablepool by slow release of nitrogen from the soil organic mat-ter. It is our current concept that there exists not one but twonitrogen cycles, one of which involves "fast" nitrogen andthe other, "slow" nitrogen. The "fast" nitrogen is thatwhich rapidly enters and leaves the microbial pool fromplant exudates and exfoliates and from the easily decom-posable constituents of plant litter. Nitrogen from this poolsupplies the bulk of the annual plant growth requirement fornitrogen in unfertilized ecosystems. The "slow" nitrogenfollows the classic concept of long-term residency in thesoil organic matter. Elsewhere, I have stated that once agiven nitrogen atom makes its initial entry into green her-bage, there is greatly increased probability that the sameatom will again enter green herbage not only in the next fol-lowing growing season, but also in the next several seasons.Nitrogen"15 data are at hand to substantiate that statement.

To summarize, whereas microorganisms have long beenused on highly esthetic substrates to make such products asyogurt and cognac and silage and light-textured bread,today the soil microbiologist is becoming increasingly in-volved in exposing such unesthetic substrates as sewage andanimal manures and food processing and sanitary landfillwastes to microbial attacks. His objectives are to make suchsubstrates less objectionable environmentally and to exploittheir residual food and energy potentials. Together withthese endeavors he is expanding his efforts to define thedominant roles of microorganisms in the functions of thebiosphere.

Addressing those of you who will be carrying on thework of our notable early American soil microbiologists, letme close with the words of that great Roman agriculturistwho, in speaking of the Lilliputian armies in the soil, stated:"Parvi illegitimi non carborundum." Let this quotationremind you that those on whom you work are not theendangered species.