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Microbiological Research 183 (2016) 26–41

Contents lists available at ScienceDirect

Microbiological Research

j ourna l h omepa ge: www.elsev ier .com/ locate /micres

acteria and fungi can contribute to nutrients bioavailability andggregate formation in degraded soils

uhammad Imtiaz Rashida,d,∗, Liyakat Hamid Mujawara, Tanvir Shahzade,alal Almeelbia,b, Iqbal M.I. Ismail a,c, Mohammad Ovesa

Center of Excellence in Environmental Studies, King Abdulaziz University, P.O Box 80216, Jeddah 21589, Saudi ArabiaDepartment of Environmental Sciences, King Abdulaziz University, Jeddah 2158, Saudi ArabiaDepartment of Chemistry, King Abdulaziz University, Jeddah 2158, Saudi ArabiaDepartment of Environmental Sciences, COMSATS Institute of Information Technology, 61100, Vehari, PakistanDepartment of Environmental Sciences & Engineering, Government College University, 38000, Faisalabad, Pakistan

r t i c l e i n f o

rticle history:eceived 13 October 2015eceived in revised form6 November 2015ccepted 21 November 2015vailable online 25 November 2015

eywords:egraded landood securityicrobial inoculautrient bioavailability

a b s t r a c t

Intensive agricultural practices and cultivation of exhaustive crops has deteriorated soil fertility and itsquality in agroecosystems. According to an estimate, such practices will convert 30% of the total worldcultivated soil into degraded land by 2020. Soil structure and fertility loss are one of the main causesof soil degradation. They are also considered as a major threat to crop production and food security forfuture generations. Implementing safe and environmental friendly technology would be viable solutionfor achieving sustainable restoration of degraded soils. Bacterial and fungal inocula have a potential toreinstate the fertility of degraded land through various processes. These microorganisms increase thenutrient bioavailability through nitrogen fixation and mobilization of key nutrients (phosphorus, potas-sium and iron) to the crop plants while remediate soil structure by improving its aggregation and stability.Success rate of such inocula under field conditions depends on their antagonistic or synergistic interac-tion with indigenous microbes or their inoculation with organic fertilizers. Co-inoculation of bacteria and

oil fertilityiderophoresoil aggregation

fungi with or without organic fertilizer are more beneficial for reinstating the soil fertility and organicmatter content than single inoculum. Such factors are of great importance when considering bacteriaand fungi inocula for restoration of degraded soils. The overview of presented mechanisms and interac-tions will help agriculturists in planning sustainable management strategy for reinstating the fertility ofdegraded soil and assist them in reducing the negative impact of artificial fertilizers on our environment.

© 2015 Elsevier GmbH. All rights reserved.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 272. Reinstating fertility of degraded soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28

2.1. Microbial inocula and soil nutrient bioavailability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292.1.1. Nitrogen fixation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 292.1.2. N2 fixation in degraded land . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29

3. Mechanisms used by microbes to reinstate the fertility of degraded soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293.1. Fungi and N fixation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29
2
3.1.1. How do fungi influence N2 fixation? . . . . . . . . . . . . . . . . . . . . .

3.2. Phosphorus mobilization. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

3.3. Potassium. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author at: King Abdulaziz University, Center of Excellence in EnvironmE-mail addresses: [email protected] (M.I. Rashid), [email protected] (M. Oves).

ttp://dx.doi.org/10.1016/j.micres.2015.11.007944-5013/© 2015 Elsevier GmbH. All rights reserved.

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ental Studies, P.O Box 80216, Jeddah 21589, Saudi Arabia. Fax: +966 12 6951674.

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M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41 27

3.3.1. Fungi and K mobilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 313.3.2. How do bacterial and fungal inocula increase K mobilization? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31

3.4. Role of bacteria in Fe mobilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 313.5. Interaction between bacteria and fungi inocula to improve nutrient bioavailability in soil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33

4. Soil structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 334.1. Bacteria and soil aggregation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 344.2. Fungi and soil aggregation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34

4.2.1. How do fungi influence soil aggregation? Mechanism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354.3. Interaction between fungi and bacteria to improve soil aggregation and their stability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35

5. Organic amendments to reinstate soil fertility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 365.1. Bacterial and fungal inocula to reinstate the fertility of degraded land . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 365.2. Application of bacterial and fungal inocula with organic amendments to reinstate the fertility of degraded land . . . . . . . . . . . . . . . . . . . . . . . . . . . 365.3. Gaps in current approaches and way forward to restore the degraded land. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .37

6. Future considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 377. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37 . . . . . .

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References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. Introduction

The global human population is increasing continuously, thatas propelled up to 7 billion at present (Godfray et al., 2010; Glick,015). At this projected growth rate, the world population will riseo about 9.5 billion by 2050, thus exerting immense pressure onood supplies (Glick, 2015). According to FAO (2009), the global foodemands in coming decades will raise by 70%, which will enhancehe need of intensively growing agricultural crops (Godfray et al.,010; Tilman et al., 2011). To encounter this issue, soils are culti-ated with extractive crops which depleted the nutrient reserveshat had led to negative balance of nutrients and soil degrada-ion (van Lynden and Odeman, 1998; Kraaijvanger and Veldkamp,014). This can be defined as physio-chemical and biological deteri-ration of soil environment through anthropogenic activity leadingo a serious decline in soil productivity and fertility (Dregne, 2002).he other dominant form of soil degradation are erosion and salin-ty, where the causative factors for former type include impropergricultural practices, deforestation and overgrazing (van Lyndennd Odeman, 1998, Fig. 1). These practices degrade 38% of theorld agricultural land, 21% permanent pasture and 18% forests

nd woodlands (Oldeman et al., 1990; Utuk and Daniel, 2015). Ofhe total degraded cropland, pasture and woodland, Oldeman et al.1990) categorized as lightly (9%), moderately (10%) and strongly4%) degraded soils. Light and moderately degraded soils are suit-ble for local farming with reduced agricultural functions. A largeecline in productivity of such soils and their restoration is possi-le with changes in farm management practices whereas severelyegraded soil virtually lose their productivity and their originaliotic functionality (Oldeman et al., 1990; Utuk and Daniel, 2015).n former soils, removal of organic matter and nutrient rich layer ofoil profile causes nutrient depletion, the loss of soil fertility, struc-ure and water holding capacity (Montgomery, 2007). Productionf agricultural crops on such soil strongly depends on the nutrientvailability and good soil structure for supporting plant growth.

Nitrogen (N), phosphorus (P), potassium (K) and iron (Fe) areey nutrients that play a major role in crop production on degradedoils. As most of the soils in the world are known to be deficient inforementioned nutrients, there will be a great demand of chemi-al fertilizers to fulfill nutrients deficiency. According to FAO (2012),y the end of 2016 the global requirement of chemical fertilizersN, P, K and other macronutrients) is expected to reach 194 mil-ion tons. Manufacturing of the chemical fertilizers to meet this
emand requires a huge amount of nonrenewable resources such asnergy in the form of oil and natural gas. In addition, excessive usef chemical fertilizers has also contributed to soil and air pollutiongreenhouse gaseous emissions) as well as water eutrophication
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38

in many parts of the world. Therefore, efforts are necessary to fig-ure out alternative, innovative, environmental friendly options toreduce the use of costly and non-environmental friendly chem-ical fertilizers. In this context, microbes (i.e., bacteria and fungi)naturally occurring in soil or supplied as bio-fertilizers, could rep-resent a promising approach to increase nutrients bioavailabilityand improve soil structure.

Bacterial and fungal inocula and organic amendments couldbe considered as a potential option to incorporate in crop inte-grated nutrient management strategy of degraded soils (Medinaet al., 2010; Chaer et al., 2011). Introduction of these inoc-ula can exploit, translocate, mineralize and mobilize soil P, K,Fe reserves, increase organic matter or fix N from the atmo-sphere (Figueiredo et al., 2011b; Ahemad and Kibret, 2014;Leifheit et al., 2014; Nguyen and Bruns, 2015; Owen et al., 2015).

According to van der Heijden et al. (2008), arbuscular mycorrhizal(AM) fungi and biological N fixing bacteria annually contribute5–20% to the total N demand of grassland and savannah. The contri-bution of AM fungi to temperate and boreal forests is 80% whereastotal P acquired by plants through bacteria and fungi was 75%.The basic mechanisms through which bacteria and fungi promotenutrients bioavailability include N fixation, P, K and Fe mobiliza-tion through production of organic acids and siderophores (Fig. 1).In addition to this, organo-polysaccharides and proteins (golma-lin, mucilages and hydrophobins) are also produced that help topromote soil aggregate stability (Fig. 1) (Mortimer et al., 2008;Glick, 2012; Caesar-Tonthat et al., 2014; Nguyen and Bruns, 2015;Owen et al., 2015). These processes are carried out by bacteria, andAM fungi. Later group of microbes form a symbiotic associationwith legume roots infected by N fixing bacteria that increase P,micro and other macronutrients for plant uptake as well as miti-gate the effect of water and salt stress (Sánchez-Díaz et al., 1990;Nadeem et al., 2009). Free-living and symbiotic bacteria enhanceplant growth by providing N through atmospheric N2 fixation andproduce (phyto)-hormone (auxins, cytokinins and gibberellins) inaddition to anti-microbial molecules to protect the crops from dis-eases (Khan, 2005).

In the past, agriculturists had immensely practiced the appli-cation of earthworms and organic fertilizers to improve the soilfertility (Rashid et al., 2013; Shah et al., 2013; Rashid et al., 2014b,2014a). Both practices prove to be beneficial for soil nutrientmanagement of agroecosystems. However, earthworm enhancedgreenhouse gaseous emissions (Lubbers et al., 2013), and their
successful functioning was achieved at an expense of maintain-ing their healthy population in soil. Such high maintenance costswould directly affect the price index of the crops. Another possibil-ity would be to improve the soil fertility by enriching the soil with

28 M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41

soil or

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Fig. 1. Mechanisms used by bacteria and fungi to improve

icroorganisms such as bacteria and fungi. These microorganismsre omnipresent and found in various components of earth such asater and soil.

Bacteria and fungi are also known to improve soil struc-ure by promoting the formation of soil aggregates and poresithin (Degens, 1997; Miller and Jastrow, 2000). Fungal cells

elease mucilaginous exudates which are mainly composed ofxtracellular surface polysaccharides; cell wall polysaccharidesnd somatic or intracellular polysaccharides located inside theytoplasmic membrane. Extracellular polysaccharides are mainlyesponsible for the formation of aggregates, which are beneficialor improving porosity and aeration in soil. Moreover, bacteriaelease exopolysaccharides that form organo-mineral complexeshich help to bind soil particles into aggregates (Degens, 1997).

xperimentally it has been proved that soil structure is not onlynfluenced by the mineral constituents of the soil but also by theresence of micro-organisms in pores (Gupta and Germida, 2015).n the other hand, exudates from bacteria, fungi, decomposed cellss well as plant and animal residues especially in soils managed byrganic inputs are also responsible to boost the soil organic matterhich in turn improve the soil structure, function and quality.

Reconnoitering the mechanisms of bacterial and fungal inoc-la together with organic fertilizer could be very valuable toolor improving soil fertility (Song et al., 2015) and aggregation.uch strategy may help in planning a chemical fertilizer-free, envi-onmental friendly integrated soil nutrient management to meetlobal food demand which may further help in reinstating theertility of degraded soil. In this regard, various aspects of theacterial and fungal-mediated soil nutrient acquisition processesnd aggregate formation have also been recognized. Co-inoculationf bacteria and fungi with organic amendments could be an elo-uent approach for sustainable management of soil fertility androp production (Minerdi et al., 2001; Rillig et al., 2002; Mortimer
t al., 2008; Caesar-Tonthat et al., 2014) in strongly degraded soil.n order to avail maximum benefits from such approaches, therere still many undeveloped facets that need to be explored inuture studies. The mechanistic understanding of bacterial and
ganic matter (SOM), nutrient availability and aggregation.

fungal-mediated soil nutrient enhancement and aggregation is stillunderdeveloped. Novel field-based studies and experiments undercontrolled conditions need to be planned to lend better accuracy inthe understanding of microbial influenced soil fertility and struc-tural attributes. The main objective of present review is to highlightand discuss current knowledge on the mechanisms used by bacte-ria and fungi inocula to influence soil nutrient bioavailability (N, P,K and Fe; other nutrient are not in the scope of this review) andaggregation. We will discuss the effectiveness of these microbeswhen inoculated solely, as co-inoculant or in combination withorganic fertilizer in improving fertility and aggregation stability ofdegraded soils.

2. Reinstating fertility of degraded soils

Land degradation is a worldwide problem caused by numberof human induced processes that result in loss of soil fertility andproductivity. The major causes of the land degradation includesdeforestation, improper agricultural practices, (intensive cultiva-tion, unbalanced fertilization, poor quality irrigation and chemicalinputs in the form of fertilizers or pesticides) and industrializa-tion (Dregne 2002). Moreover, Dlamini et al. (2014) have associatedland degradation with decrease in soil organic carbon and N stocks.According to estimation by Bai et al. (2008), about 40% of the worldagricultural soils are seriously degraded whereas 24% area of theproductive soils is still under continuous degradation. This requiresspecial attention to figure out alternative and sustainable nutrientmanagement techniques that can reinstate the fertility of such soils.Integrated management of microbial inocula and organic fertilizerscould be an alternative option which needs to be explored in futurestudies. In the following sections, few approaches for restoring thefertility of degraded soils are discussed. However, the limited focus
of following discussion will not provide complete guidelines forattaining sustainable restoration of degraded soil, but it describesfew essential management options that could be important to con-sider in this regard.

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M.I. Rashid et al. / Microbiol

.1. Microbial inocula and soil nutrient bioavailability

Various species of bacteria and fungi play a key role in improv-ng soil fertility. These microbes increase organic matter that boostshe availability of N, P, K and Fe in soil (Egamberdiyeva and Höflich,004; Caesar-Tonthat et al., 2014; Leifheit et al., 2015). Additionally,hey also produce organic acids for the mobilization of nutrientsnd facilitate their plant uptake from the rhizosphere. The simi-arities or differences in bacteria and fungi to influence nutrientioavailability and aggregate formation are discussed in Table 1.n this manner, the application of chemical fertilizers in agro-cosystems can be greatly reduced (Figueiredo et al., 2011a). Hence,pplication of microbial inocula would not only help the farmers toeduce the additional costs of chemical fertilizers but also assistn obtaining high crop yield. Most of the processes through which

icrobial inocula promote soil fertility are not fully understood,owever it is believed that microbes use several direct and indirectechanisms (Glick, 2012). These are highlighted and reviewed in

orthcoming sections.

.1.1. Nitrogen fixationNitrogen (N) is an essential nutrient required by plants for

heir growth and metabolism. It is often lost through leaching ormission thus limiting its availability in most of the cultivatedoils. Although N is present abundantly in atmosphere in the formf diatomic (N2) molecule, but its structure makes N2 moleculenert. However, reduction of N2 molecule into N is a complex pro-ess which requires input of huge amount of energy (Postgate,982). Prokaryotic microorganisms known as diazotrophs fix atmo-pheric N2 in the form of ammonia (NH3) through their normaletabolic process (Riggs et al., 2001; Galloway et al., 2008). Theseicrobes are free living organisms present in the bulk soil (Reed

t al., 2011) that mainly includes Cyanobacteria, Proteobacteria,rchaea, and Firmicutes (Demba Diallo et al., 2004; Duc et al., 2009).ome of these organisms (Azotobacter and Azoarcus genera) arelso present at comparable densities in the rhizosphere and bulkoil. However, there are other bacteria from genera Herbaspirillumnd Azospirillum that colonize only in the rhizosphere (Mrkovackind Milic, 2001; Malik et al., 2002; Bashan et al., 2004; Bashannd De-Bashan, 2010). Rhizobia has the capability to infect rootsnd induce the formation of root nodules (Stacey, 2007). There-ore in the field of N fixation, most of the researchers speciallyocus on rhizobium-legume symbiosis due to higher impact onrimary productivity of the agricultural ecosystem (Rengel, 2002).he establishment of this association results in the formation ofighly specialized organ called ‘nodules’ that are formed on the

ntracellular root of symbionts, on which bacteria colonize. Suchacteria mainly belong to the family Rhizobiaceae that develop aighly specific interaction with the infected root. This interactiononsists of several stages which involves the exchange of complexignals between the bacterium and plant (Sprent et al., 1989). Bac-eria fix N2 through a complex enzyme system called nitrogenaseKim and Rees, 1994) and this enzyme system exists as two sep-rable components; (1) dinitrogenase reductase (Fe-protein) and2) dinitrogenase metal cofactor. The former enzyme serves as anxclusive electron donor with high reducing power whereas theater (substrate reduction component) accepts the electrons energynd convert inert N2 molecule into NH3. In order to produce oneole of NH3, 16 moles of adenosine triphosphate (ATP) is required

y these microbes (Hubbell and Kidder, 2009), who obtain thisnergy by oxidizing organic molecules. Free-living bacteria mustbtain this amount of ATP from other organisms, while photo-
ynthetic microbes (cyanobacteria) use self-generated energy fromhotosynthesis process. Other microbes like associative and sym-iotic nitrogen-fixer get these compounds from the rhizospheref their host plant (Hubbell and Kidder, 2009). The chemical reac-
Research 183 (2016) 26–41 29

tion of microbial N fixation (Postgate, 1998) is shown in followingequation.

N2 + 8 H+ + 8e− + 16MgATP → 2NH3 + H2 + 16MgADP + 16Pi

2.1.2. N2 fixation in degraded landPhosphorus (P), potassium (K) and sulphur are generally lim-

ited in degraded soils. Under nutrient limited conditions, thesenutrients affect the N2 fixation by reducing the growth of N-fixingbacteria, nodule formation and functioning, as well as affectinghost plant growth. Meta-analysis study of Divito and Sadras (2014)confirmed that nodule production, activity and their number arelimited more than plant shoot biomass in response to the deficiencyof P, K and sulphur. Moreover, P limitation in soil decreases theactivity of nitrogenase enzyme in N-fixing bacteria, because bothautotrophic and heterotrophic bacteria require high ATP for cellu-lar N2 fixation (Reed et al., 2007, 2011; Pérez et al., 2014). Similar tonutrient deficiency, soil moisture is another major factor that influ-ences nodule formation or retardation of nodule growth. Wateravailability in soil is related to water holding capacity which is verylow in degraded soil (Montgomery, 2007). According to Sinclairet al. (1987) water limiting conditions severely affect nodule for-mation in soybean crop. Thus in degraded soils, N2 fixation andother related functions (decomposition, mineralization, enzymesor organic production) of microbes are severely affected due to lossof fertility and water holding capacity. Soil microbes adapt vari-ous strategies to cope with such deficiencies. These strategies arediscussed in the forthcoming sections.

3. Mechanisms used by microbes to reinstate the fertility ofdegraded soils

3.1. Fungi and N2 fixation

In light and moderately degraded soils, AM fungi play an impor-tant role in N2 fixation by providing favorable environment for thebacteria to infect plant root. As indicated by Puppi et al. (1994) andNasto et al. (2014), AM colonization can fulfill high demands of Prequired by nitrogenase enzymes for N2 fixation when inoculatedwith N2 fixer rather than non-N2 fixer to increase the growth ofhost plant. Many studies reported that co-inoculation of bacteria orlegumes with AM fungi increased N2 fixation ability of legumes ortrees (Ibijbijen et al., 1996; Bona et al., 2014). However, this increasein N2 fixation ability does not necessarily mean that growth andproductivity of host plants will increase. Meta analyses studies byLarimer et al. (2010) and Kaschuk et al. (2010) have shown thatco-inoculation of AM fungi with rhizobia or free living N-fixingbacteria resulted in a non-additive effect on the growth of hostplant. However, plant growth responses were positive when AMfungi or N2 fixer were inoculated alone. Extra-radical hyphae of AMseem to have ability to fix atmospheric N2 through N-fixing bacteriapresent in mycelia. According to Bianciotto et al. (1996) and Minerdiet al. (2001), extra-radical hyphae of AM fungi have the poten-tial to protect the intracellular bacteria of the genus Burkholderia.One of the most important ecological significance of these bacte-rial genera associated with fungi is to have the potential abilityto fix atmospheric N2, either in the nodules or as free living form.In this association, bacteria reside in the thickest host structures(i.e. mycelium) to shelter the enzyme complex from oxygen and fixatmospheric N2 in this structure (Minerdi et al., 2001). However,
the mechanism to fix N2 in the mycelium (Kneip et al., 2007), stillneeds to be determined and need continuous research efforts tofocus on this area especially for the recovery of nutrient depleteddegraded soils.


Table 1Differences in bacteria and fungi for nutrient bioavailability and aggregate formation.

No. Nutrient/structure Bacteria Fungi

1 Nitrogen (N) Diazotrophs fix N2 as ammonia through their metabolicprocess. Bacteria from family Rhizobiaceae living in the soilinfect plant root to form nodules and fix N in this structurethrough complex enzymes system.

Fungi do not fix N but provide growth limiting nutrients (i.e.,carbon and P) to bacteria for N fixation. Also, in mycelium,fungi provide shelter to bacterial enzyme system from O2 to fixN.

2 Phosphorous (P) P solubilization or availability is enhanced by P mineralizationas well as well as production of siderophores and organic acidsin the soil.

Increase P bioavailability through mineralization in soil,mycelial transport, P solubilization by siderophores, Nassimilation and CO2 release.

3 Potassium (K) Bacteria release various types of organic acids to solubilize K inthe soil through various processes such as acidolysis, chelation,complexolysis and exchange reactions.

Influence K mobilization through mycelial transport as well asby K solubilization process that involves the release of H+, CO2

and organic acid such as citrate, malate and oxalate.4 Iron (Fe) Production of siderophores which has affinity to chelate and

solubilize iron from mineral or organic compounds.Translocate Fe from mineral to organic soil horizon fordecomposition and mineralization, and release chelator(siderophores) for Fe translocation in soil.

5 Aggregate formation Produce peripheral slime polymers and decompose organict are

Hyphal network entrap soil particle and forces them together.

3

bcfiaclafNraoDaatcOwtbntceionostdM

3

ebairPvr

material to form organo-mineral products thawith soil particles to form aggregates.

.1.1. How do fungi influence N2 fixation?As discussed above, fungi indirectly affects N2 fixation through

acteria present in mycelia. During this process, fungi translocatearbon and P from the plant roots to the associated bacteria for N2xation. In this regard Paul and Kucey (1981) observed a symbioticssociation of bacteria and fungi with legumes, which may indi-ate a competition between these microbes for carbon provided byegume roots. However, this competition is masked by the associ-tion of AM fungi with Rhizobia who provides a high amount of Por nitrogenase enzyme complex (Puppi et al., 1994). The enhanced

2 fixation ability of the bacteria through AM association is dete-iorated by the depletion of P zone in mycorrhizosphere. AM fungilso provide plant derived carbon to increase the potential abilityf non-symbiotic N2 fixer such as Herbaspirillum and Azospirillum.uring this association, AM fungi decrease the total amount of sugarnd enhance nitrogenous compounds in mycorrhizosphere (Jonesnd Oburger, 2011). The changes occurred in this region strengthenhe carbon limitation of N2 fixer over other microorganisms whichould limit their performance to fix N2 (Veresoglou et al., 2012).n the other hand, non-symbiotic N2 fixer are versatile organismshich possess the ability to adapt the carbon and N limiting condi-

ions (Blaha and Schrank, 2003). Their performance is not affectedy the changes that occur in rhizosphere due to AM fungi colo-ization (Veresoglou et al., 2012). Therefore, it is not always truehat AM fungi association with plant and rhizobia would be benefi-ial for long term recovery of degraded land as proposed by Chaert al. (2011). In such condition, carbon limitation could be replen-shed by organic amendments in addition to the synergistic effectf co-inoculants such as N-fixing bacteria and AM fungi. Such phe-omenon needs to be further investigated for sustainable recoveryf degraded soils. In this regard, efforts are done to figure out theole inoculation of N-fixing bacteria or AM fungi with organic fer-ilizers and obtained encouraging results for the rehabilitation ofegraded land under semi-arid environment (Medina et al., 2010;engual et al., 2014a; Mengual et al., 2014b).

.2. Phosphorus mobilization

Phosphorus (P) is another essential and growth-limiting nutri-nt in agro-ecosystems (Smil, 2000). However, this limitation coulde fulfilled by external inputs to the soil in the form of organics well as synthetic fertilizers (Fig. 2). The later form of fertilizers formulated from the rock phosphate reserves. Therefore, many
esearchers are concerned about rapid diminution of the world’s
reserves due to continuous mining for P (Cordell et al., 2009;an Vuuren et al., 2010). Recently, there is a contradiction in viewsegarding the availability of world P reserves. Simulation studies

associated Production of mucilages, polysaccharides and extracellularcompounds as well as soil proteins such as glomalin andhydrophobins.

suggested that global P production will reach to maximum by 2033(Cordell et al., 2009) while other researchers had concluded thatalmost 50% of the currently available P reserves will be mined by2100 (van Vuuren et al., 2010).

In most of the agricultural soils (productive or degraded), hugereserves of inorganic or organic P are present in immobilized orunavailable form. Fonte et al. (2014) observed no difference intotal P in degraded and productive pasture, however in this study,organic P was 40% higher in latter pasture soil. They explained thisby showing the presence of higher inorganic P in degraded thanproductive pasture which was strongly adsorbed or occluded inthis soil. In fact, inorganic P is highly reactive with some metal com-plexes such as iron, aluminum and calcium (Fig. 2), which lead to75–90% of P adsorption or precipitation in the soil (Igual et al., 2001;Gyaneshwar et al., 2002); Fig. 2). Even after the application of P fer-tilizers to the soils, a very low amount (micromolar) of P is availableto plants as most of the P is adsorbed or becomes sparingly soluble(Gyaneshwar et al., 2002); Fig. 2). Microbial inocula such as bacteria(Han and Lee, 2005; Tao et al., 2008; Chang and Yang, 2009; Ma et al.,2009; Yadav et al., 2014) mobilize native and inherited soil P as wellas any applied insoluble finely ground rock P. Such type of inoculaare now termed as P-mobilizing microbes (Owen et al., 2015) ratherthan previously referred as phosphate-solubilizing microorgan-isms (Rodrııguez and Fraga, 1999; Rodriguez et al., 2004; Dastageret al., 2010; Jones and Oburger, 2011). As these inocula do not onlysolubilize P, but they also mobilize its organic form through miner-alization (enzymatic hydrolysis) and facilitate the translocation ofphosphate (Owen et al., 2015); Fig. 2). Microbes are responsible formobilizing the soil P unavailable for plants through their direct andindirect effects. In direct processes, (i) microbes solubilize P by low-ering the pH (through proton extrusion) of external medium andproducing low molecular weight organic anions (Fig. 2) like suc-cinic, citric, gluconic, �-ketogluconic and oxalic acids (Chen et al.,2006). These anions are exchanged for P on adsorption sites of soil,the process commonly referred to as ligand exchange (Jones andOburger, 2011; Zhang et al., 2014). Hydroxyl and carboxyl groupsof these acids chelate the cations bound to phosphate thereby con-verting it to soluble forms (Miller et al., 2010). (ii) In addition,the inocula hydrolyze organic P compounds by producing phos-phatases or phytases (Fig. 2). Besides there are several ways throughwhich indirect mobilization of P can be carried out by these inoc-ula: (i) Microbes release CO2 during respiration which is dissolvedin water (present in the soil pores) to form carbonic acid, thus sol-
ubilizing P by decreasing the pH of mycorrhizosphere (Marshner,1995) (ii) Microbes release proton (H+) during assimilation of NH4
+

as a result of which the soil pH is lowered and hence solubilize theavailable P (Illmer and Schinner, 1992) (iii) P solubilizing microbes


F ents (

t Sp

hit

3

pibcm2adfcwpKueaoia(icftH

3

fceo

ig. 2. An overview of the mechanism used by bacteria and fungi to mobilize nutri

o enhance nutrient bioavailability. Specifies primary intermediary steps.

ave the ability to remove and assimilate phosphate from the soiln order to re-establish the P equilibrium, in this way they stimulatehe indirect dissolution of Ca–P (Halvorson et al., 1990); (Fig. 2).

.3. Potassium

Potassium (K) is another vital nutrient and considered as a keyarameter of soil fertility and plant growth. In most of the soils, K

s present in very small amount ranging from 0.04 to 3%. Despiteeing in limited amount, 98% of this K is bound within phyllosili-ates structure (Shelobolina et al., 2014). This is the layer of silicateinerals found in silt and clay fractions of the soil. The remaining

% exists in soil solution or on exchange sites to become avail-ble for the plants (Sparks and Huang, 1985). Hence, soil fertility isecreased due to low availability of this nutrient which is normallyulfilled by commercial fertilizer (i.e., KCl), thus elevating the inputost of the farmers. Recently, few microbial strains were isolatedho had an ability to oxidize in the first step Fe2+ from primaryhyllosilicates mineral in such a way that they release iron and

from these minerals (Shelobolina et al., 2014). Bacterial inoc-la (Neutrophillic lithotrophs) utilize structural Fe2+ in biotite as anlectron donor for their metabolism in order to produce energynd oxidize biotite (Shelobolina et al., 2014). The microbes whichxidized biotite (Fe2+-bearing mica) include Bradyrhizobium japon-

cum, Cupriavidus necator, Ralstonia solanacearum, Dechloromonasgitate, and Nocardioides sp . In addition to this, Sheng and He2006) suggested that inoculation of B. edaphicus NBT strains andts mutants increase the production of citric, oxalic, tartaric, suc-inic, and �-ketogluconic acid. These acids lead to K mobilizationrom K-containing minerals (e.g. mica, biotite, kaolinite and smec-ite) and chelation of silicon ions (Han and Lee, 2005; Sheng ande, 2006).

.3.1. Fungi and K mobilizationIn addition to bacterial strains, mineral form of K is solubilized by

ungi through releasing organic acid anions which mainly includesitrate, malate and oxalate (Meena et al., 2014). According to Wut al. (2005), K uptake was increased in corn crop after inoculationf G. mosseae (now, Funneliformis mosseae) and G. intraradices (now,

P, K and Fe) in the soil. Indicates processes carried out by microbial inocula

ecifies secondary intermediary steps. Microbial inoculum.

Rhizoglomus intraradices) (Sieverding et al., 2014). In degraded soil(acidic), K solubilization was higher than calcium and magnesiumafter inoculation of AM fungi compared to un-inoculated control(Clark et al., 1999). Inoculation of Aspergillus terreus and Aspergillusniger increased the K level in soil solution by solubilizing K frominsoluble feldspar and potassium aluminum silicate (Prajapati et al.,2012). This was related to the production of organic acids espe-cially by A. terreus which shows higher K solubilization than A.niger . Moreover, other studies have reported that A. niger also pro-duce organic acids and trace elements during rock solubilization(Vandenberghe et al., 1999; Mirminachi et al., 2002).

3.3.2. How do bacterial and fungal inocula increase Kmobilization?

The major processes involved in mobilizing K are acidolysis andcomplexolysis exchange reactions (Uroz et al., 2009). During aci-dolysis, soil inocula such as bacteria or fungi decrease the local pHby producing succinic, citric, gluconic, �-ketogluconic and oxalicacids (Fig. 2). Production of protons (H+) and organic acids anionsnot only enhances the chelation of cations which are bound to K butalso helps for acidolysis of surrounding environment of microbes(Uroz et al., 2009; Zarjani et al., 2013; Parmar and Sindhu, 2013).During the process of acidolysis, rhizospheric microbes can chelateAl and Si cations associated with K minerals and by doing so theyalso enhance the exchangeable K in soil solution (Römheld andKirkby, 2010). Consequently, microbes not only synthesize but alsodischarge H+, inorganic and organic acids to acidify their own cells,rhizosphere and surroundings of K minerals. This play an impor-tant role in mobilizing or solubilizing insoluble form and structuralunavailable forms of K compounds in to soil solution resulting anincreased K availability in rhizosphere (Goldstein, 1994; Abou-el-Seoud and Abdel-Megeed, 2012).

3.4. Role of bacteria in Fe mobilization

Iron is the fourth most abundant element available on earthand predominantly exists in nature in ferric (Fe3+) form. It isconsidered as one of the key micronutrient for soil fertility andis also needed by all kind of living organisms. It is sparingly

32

M.I.

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et al.

/ M

icrobiological R

esearch 183

(2016) 26–41

Table 2Examples of various bacterial strains involved in improving soil fertility parameters.

No. Bacteria N P K Fe OM OA Reference

1 Rhizobacteria√

– – –√

– Song et al., (2015)2 Pseudomonas aeruginosa BS8

√ √–

√– Hydrocyanic acid Goswami et al., (2015)

3 Bradyrhizobium diazoefficiens USDA110 and B.japonicum THA6√

– – –√

– Prakamhang et al., (2015)4 Pseudomonas aeruginosa Azotobacter chroococcum Azospirillum brasilense –

√– – – – Yadav et al., (2014)

5 Bradyrhizobium japonicum UCM B–6018√ √ √ √

– Free amino acids Tytova et al., (2013)7 B. megaterium –

√– – – – Han and Lee, (2005)

8 B. mucilaginosus –√

– – – – Han and Lee, (2005)9 B. edaphicus – –

√– – Citric, oxalic, tartaric, succinic, and �–ketogluconic acids Sheng and He, (2006)

10 Pseudomonas strain GRP3√

– –√

– – Sharma et al., (2003)11 Pseudomonas fluorescens C7

√– –

√– – Vansuyt et al., (2007)

12 Klebsiella pneumonia, Pantoea agglomerans√

– – – – – Riggs et al., (2001)13 Azotobacter spp

√– – – – – Mrkovacki and Milic, (2001)

14 Azotobacter chroococcum√

– – – – – Wu et al., (2005)15 Pseudomonas alcaligens PsA15

√– – – – – Egamberdiyeva and Höflich, (2004)

16 Mycobacterium phlei MbP18√

– – – – – Egamberdiyeva and Höflich, (2004)17 Azospirillum spp.

√– – – – – Bashan and De–Bashan, (2010)

18 Azospirillum lipoferum, Azospirillum brasilense√

– – – – – Malik et al., (2002)19 Bacillus spp, Burkholderia spp –

√– – – Tao et al., (2008)

20 Streptomyces spp. –√

– – – – Chang and (Yang, 2009)21 Achromobacter spp. –

√– – – – Ma et al., (2009)

22 Microccocus spp. –√

– – – – (Dastager et al., 2010)23 Azospirillum spp. –

√– – – Gluconic acid Rodriguez et al., (2004)

24 Bacillus megaterium –√

– – – – Wu et al., (2005))25 Pseudomonas alcaligenes –

√– – – – Zhang et al., (2014)

26 P. natatu –√

– –√

– Cui et al., (2015)27 S. guianensis –

√– –

√– Cui et al., (2015)

28 Bacillus mucilaginous√

– – – – – Han and Lee, 2005; Wu et al., (2005)29 B. megaterium

√– – – – – Han and Lee, (2005)

31 Pseudomonas spp., Erwinia herbicola, Pseudomonas cepacia, and Burkholderia cepacia – – – – – Gluconic acid Rodrııguez and Fraga, (1999)32 Rhizobium leguminosarum

√ √ √ √– – Biswas et al., (2000)

N = Nitrogen, P = phosphorous, K = potassium, OM = organic matter, OA = organic acids. –N/A√Positive effect of inoculant.


Table 3Examples of various fungal strains involved in improving soil fertility and structural parameters.

No. Fungi N P K OM AF/GP AS Reference

1 Rhizophagus irregularis – – –√ √ √

Leifheit et al., (2015)2 Agaricus lilaceps – – – –

√ √Caesar–TonThat et al., (2013)

3 Paraglomus occultum – – –√ √ √

Wu et al., (2014)4 Glomus mosseae

√ √–

√ √ √Xu et al., (2015)

5 Laccaria bicolor, L.laccata, Lactarius theiogalus, Paxillus involutus and Suillus bovinus – – – –√ √

(Zhang et al., 2014)6 R. intraradices, G.aggregatum, G.viscosum, Claroideoglomus etunicatum, C.claroideum

√ √ √– – – Bona et al., (2014)

7 G. mosseae and G. intraradices – –√

– – – Wu et al., (2005)8 Aspergillus terreus and A. niger – –

√– – – Prajapati et al., (2012)

N rmati–√

smdv2tzepiasUteCaudepo2Nti2caat

3n

nRpbs2awrathifa

= Nitrogen, P = phosphorous, K = potassium, OM = organic matter, AF = aggregate foN/APositive effect of inoculant .

oluble, therefore not readily available for plant or other biota likeicrobes in aerated soil. Moreover, in soil, ferrous (Fe2+) is oxi-

ized to Fe3+ thereby forming insoluble compounds and leaving aery low amount of iron for microbial or plant assimilation (Ma,005). Therefore, to fulfill iron requirement for normal growth,ough competition exists among bacteria, fungi and plant in the rhi-osphere. In such circumstances, some strains of bacteria (Sharmat al., 2003; Vansuyt et al., 2007) synthesize low-molecular massroteins known as siderophores. These molecules have high affin-

ty to chelate (Machuca et al., 2007; Miethke and Marahiel, 2007)nd solubilize iron from mineral or organic compounds. Generally,iderophores have high affinity to form complexes with Fe3+ (1:1).ptake of the complexes by the cell membrane of both Gram posi-

ive and negative bacteria reduces Fe3+–Fe2+. Later cell membranexpel these ions from the siderophores into the cell (Boukhalfa andrumbliss, 2002) by linking its inner and outer membranes, a mech-nism called “gating”. In this way siderophores solubilize iron fromnavailable minerals or organic compounds in iron limited con-ition (Indiragandhi et al., 2008). Additionally, bacteria producextracellular siderophores which deprive pathogenic organismsroduced under Fe limited condition and form complexes withther heavy metals (Zn, Pb, In, Cu, Ga, Cd and Al) (Schalk et al.,011) and radionuclides including U and Np (Kiss and Farkas, 1998;eubauer et al., 2000). Presence of such heavy metals encourages

he bacteria to produce siderophores which chelate the metal toncrease Fe availability in the rhizosphere of these soils (Wang et al.,002). Such bacteria play a vital role in elevating heavy metal con-entration by phytoextraction through enhancing the activity ofntioxidants. Hence, siderophores produced by microbial inoculalso play a key role in alleviating the stresses imposed on plantshrough heavy metals.

.5. Interaction between bacteria and fungi inocula to improveutrient bioavailability in soil

Fungi and bacterial inocula interact with plant roots to improveutrient availability in soil for plant uptake (Glick, 1995; Smith andead, 2010; Prakamhang et al., 2015); Tables 2 and 3). For this pur-ose, the co-inoculation between bacteria–bacteria, fungi–fungi oracteria–fungi species is also significantly acknowledged in recenttudies (Tytova et al., 2013; Leifheit et al., 2015; Nguyen and Bruns,015; Ortiz et al., 2015; Prakamhang et al., 2015). In these inter-ctions, mycelium of AM fungi release carbon compounds whichill act as energy source for soil microorganisms in the mycor-

hizosphere, though the carbon products are in small amount thanlready present in rhizosphere (Andrade et al., 1997). Similarly, bac-eria also exude carbon compounds which increase the AM fungi
yphal growth and its root colonization (Barea et al., 2005). Dur-
ng the interaction among Rhizobia, AM fungi and legume, AMungi enhance the growth and yield of legume by providing waternd nutrients, especially P which increases Rhizobium N2 fixation

on, GP = glomalin protein, AS = aggregate stability.

through influencing energy production pathways (Minerdi et al.,2001; Mortimer et al., 2008). Bacteria enhance P availability foruptake of AM fungi and plant through phosphatase enzyme andorganic acid production in the soil (Owen et al., 2015). Thus, theirco-inoculation tends to increase P and N availability in soil (Table 4).Both fungi and bacterial inocula increase the nutrient availabil-ity in the soil solution through organic matter decomposition, Nfixation, P, K and Fe mobilization (Fig. 2). For instant, effect ofco-inoculation of plant growth promoting bacteria and Bradyrhi-zobium increase the soybean seed yield up to 44% per hectare thantheir lone (single) inoculant form (Prakamhang et al., 2015). Sim-ilarly co-inoculation of B. thuringiensis or Ps. putida with AM fungiincrease P by 44 and 35% in Trifolium repens respectively, while Kcontent was increased by 128 and 285%, than their lone inocula-tion (Oritz et al., 2015; Table 4). Hence, interactions among soilmicrobes in the soil rhizosphere positively affect soil fertility andprovide highly valuable ecosystem services. Therefore use of theseinocula can be exploited in order to increase yield, reduce chemicalinputs, and develop an efficient form of sustainable fertilizer man-agement in agro-ecosystems (Bhattacharjee et al., 2008; Nguyenand Bruns, 2015; Owen et al., 2015) especially in degraded soils.

In general, it is very clear from the above mechanistic discus-sion that lone microbial inoculum could not be very effective ininfluencing the bioavailability of various nutrients (Table 4); there-fore co-inoculation of microbes could prove to be more beneficialin recovery of degraded soil. However, some strains of bacteriaor fungi can possess more than one mechanism and may proveto withstand under water limited or nutrient depleted condition,therefore could be potential option for reinstating the lost functionsof degraded soils.

4. Soil structure

Destruction of soil structure is one of the most important indi-cator of soil degradation which is mainly caused by loss of organicmatter through intensive soil management practices and land usechanges (Oldeman et al., 1990; Montgomery, 2007). However, soilstructure plays a central role in crops management and thus agri-cultural ecosystems sustainability (Rillig et al., 2002). This canbe defined as size, shape and three dimensional arrangementsof organic or mineral complexes (aggregates) and pores in sucha manner that affect pore continuation, water infiltration andwater holding capacity (Bronick and Lal, 2005). According to Tisdall(1994), soil structure is an arrangement of individual soil parti-cles formed from sand, silt and clay. These are bound togetherthrough organic, inorganic or chemical forces in order to formaggregates. Single particles adhere together more strongly with
surrounding particles to form micro-, (<250 �m) and macroag-gregates (>250 �m diameter) size fraction (Kemper and Rosenau,1986). Soil aggregates support root growth, a wide array of soilfunctions and ecosystem processes. These include carbon storage


Table 4Comparative analysis of microorganisms as single inoculant and efficiency (%) when co-inoculated in the soil in absence or presence of organic fertilizer in stimulating soilfertility and structural parameters.

No. Microorganisms N P K OM AF/GP AS Reference

Single inoculant1 i. Bacillus megaterium,

ii. Bacillus thuringiensisiii. Ps Putida

√ √ √ √ √ √Ortiz et al., 2015)

2 i. Bacillus megateriumii. AM fungi

√ √ √– – – (Armada et al., 2014)

3 i. Bacillus megaterium,ii. Bacillus thuringiensisiii. Enterobacter s

√ √ √ √ √– (Mengual et al., 2014a)

4 i. Rhizophagus irregularisii. Natural soil microbes

– – – –√ √

(Leifheit et al., 2015)

5 i. Piriformospora indicaii Pseudomonas R81

√ √– – – (Kumar et al., 2012)

Co-inoculant1 Bacillus megaterium + AM fungi + compost +1 -3 +2 – – – (Armada et al., 2014)2 Azospirillum brasilense + Pantoea dispersa + organic olive residue +13 -29 +67 +8 – – (Mengual et al., 2014b)3 ii. Ps Putida + AM Fungi (Rhizophagus intraradices) – +12 +248 – – – (Ortiz et al., 2015)4 Bacillus megaterium + AM fungi +7 -42 +16 – – – (Armada et al., 2014)5 Azospirillum brasilense + Pantoea dispersa +8 +133 +84 +1 – – (Mengual et al., 2014b)6 Rhizophagus irregularis + natural soil microbes – – – – – +1 (Leifheit et al., 2015)7 Piriformospora indica + Pseudomonas R81 +21 +29 +12 – – – (Kumar et al., 2012)

Single/co-inoculant + organic fertilizer1 Bacillus megaterium + AM fungi + compost +1 −3 +2 – – – (Armada et al., 2014)2 Azospirillum brasilense + Pantoea dispersa + organic olive residue +13 −29 +67 +8 – – (Mengual et al., 2014b)3 i. Bacillus megaterium + sugar beet residue +13 +25 +14 −6 −14 – (Mengual et al., 2014a)4 ii. Bacillus thuringiensis + sugar beet residue +18 +42 −21 0 +42 – (Mengual et al., 2014a)5 iii. Enterobacters + sugar beet residue +19 +24 −3 −6 +61 – (Mengual et al., 2014a)

N rmati√

aSsaidcagi2aawboairAme

4

ttotda(a

= Nitrogen, P = phosphorous, K = potassium, OM = organic matter, AF = aggregate foPositive effect of inoculant .

nd resistance to erosion (Jastrow et al., 1998; Six et al., 2004).oil structure is mainly articulated by the degree of aggregatetability (Amezketa, 1999). Organic matter is one of the maingents in aggregate formation and stabilization. Therefore, increas-ng organic matter in soil is very vital for the rehabilitation ofegraded soils. Other factors involved in this process are persistentementing agents like humic acid that stabilizes microaggregatesnd polysaccharides derived from plants as well as microbes. Fun-al hyphae, plant roots and bacteria are temporary binding agentsn the formation and stabilization of macroaggregates (Tang et al.,011). A critical aspect in this regard is the formation of water stableggregates which are part of the macroaggregates (>250 �m). Theyre known to remain stable and fail to dissociate with frequent soiletting and drying cycles (Sun et al., 2014). Soil aggregation sta-

ility is a multifaceted process and is an indicator of many aspectsf soil structure including erosion, soil water regime and nutrientvailability. The stability of aggregates is controlled by soil phys-cal, chemical, and/or microbial community properties and plantoots (Zadorova et al., 2011; Graf and Frei, 2013; Pérès et al., 2013).mong soil microbes, AM Fungi symbionts typically represent aajor force in stabilizing macroaggregates than bacteria (Tang

t al., 2011; Leifheit et al., 2014) which stabilize microaggregates.

.1. Bacteria and soil aggregation

Influence of bacteria on soil aggregation is dependent on soil tex-ure and nutrient availability (Degens, 1997). They reside mainly inhe form of individual cells, microcolonies or biofilms in the aque-us solution within the pores of soil aggregates, thus ensuring thathey may attach to surfaces of microaggregates (Fig. 3). Bacteria
ecompose organic material to form organo-mineral products thatre associated with soil particles to form stable microaagregates2–20 �m diameter) (Tisdall, 1994). These small microaggregatesre in turn bound by bacterial and saprophytic fungi products to
on, GP = glomalin protein, AS = aggregate stability. –N/A

form slightly larger aggregates (20–250 �m diameter) (Miller andJastrow, 2000). Moreover, during bacterial growth, extracellularpolymeric substances are produced in the form of peripheral slimepolymers into soil solution (Aspiras et al., 1971); Fig. 3). These arenegatively charged polysaccharides, polyuronic and amino acidswith adhesive properties capable of making bond between clay par-ticles in order to form aggregates (Tang et al., 2011; Caesar-Tonthatet al., 2014). These aggregates adhere together to form macroaggre-gates (>250 �m diameter) and thus increase inter-particle cohesion(Degens, 1997).

4.2. Fungi and soil aggregation

The omnipresent AM fungi use its extra-radical hyphae(mycelium) to stabilize soil aggregates (Rillig et al., 2006; Bediniet al., 2009; Peng et al., 2013) as well as it can modify the mor-phological structures and biochemical nature of host plants (Borieet al., 2008) including its roots and rhizosphere. Additionally, AMFungi can also alter soil microbes in its surrounding environment aswell as the rhizosphere of host plant which are probably involvedin soil aggregation (Mansfeld-Giese et al., 2002; Rillig et al., 2006;Caesar-TonThat et al., 2007). These contributions of AM fungi areoften entangled together (Kohler-Milleret et al., 2013). According toBedini et al. (2013), mean weight diameter of aggregate (an indica-tor of stability) is strongly correlated with hyphal length of fungi butweakly with root volumes. On the other hand Glomus geosporum, F.mosseae, or G. intraradices (now R. intraradices) do not affect aggre-gate size distribution and stability in sandy loam soil (Martin et al.,2012). Daynes et al. (2013) developed a model for soil aggregation
where their simulated results indicate that AM fungi, organic mat-ter and plant roots are key contributors to aggregate formation insoil. They also observed that this group of fungi plays an importantrole in stabilization of soil aggregates.


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or two components. Instead, the process is cumulative involvingvarious factors such as plant root, soil biota (microbes and animal)and organic matter that could be enhanced by activities of soil life

Fig. 3. An overview on the role of bacterial an

.2.1. How do fungi influence soil aggregation? MechanismMycelium of AM fungi impacts soil aggregation through com-

licated direct and indirect mechanisms which are stronglynterdependent (Fig. 3). In direct mechanism, hyphal network ofM, ectomycorrhizal, saprophytic and others fungi entraps soilarticles and forces them together (Tisdall, 1994; Peng et al.,013; Zheng et al., 2014). On the other hand, Chenu et al., 2002eported that hyphal network aligns soil particles along its expand-ng hyphae to form aggregates (Fig. 3). During indirect mechanism,

ycelium exudes glomalin, hydrophobins and related soil proteinss well as mucilages, polysaccharides and extracellular compoundnto the soil (Rillig et al., 2006; Caesar-TonThat et al., 2013). Accord-ng to Driver et al. (2005), about 80% of glomalin protein is boundn hyphal wall which helps in transporting nutrients and water forM fungi. It protects the fungal hyphae and lipid rich spores fromrought and microbial attack which form clumps of soil aggre-ate through decomposed hyphae, glomalin protein fused withinerals (sand, silt and clay) and organic matter (Borie et al.,

008). Glomalin is hydrophobic protein which contributes to theydrophobicity of soil aggregates. In addition to this, the glue-likeature of glomalin also helps in the initiation and stabilization ofggregates (Miller and Jastrow, 2000) and may act as adhesivegent to bind soil particles together (Chenu, 1989; Wright andpadhyaya, 1996). Saprotrophic fungi produce extracellular exu-ates that promote water stable aggregates (Ambriz et al., 2010).imilarly extracellular mucilages like polysaccharides exuded byasidiomycetes and Trichocomaceae bind the soil particles intoggregates and increased their stability (Caesar-TonThat, 2002;aynes et al., 2012). Some species of ectomycorrhizal fungi exudesydrophobic compounds which are important in exploring largeistance in the soil for transporting nutrients and water for fungiAgerer, 2001) Fig. 3). Hydrophobins are small proteins, consideredo affect soil wettability and water repellency from the aggregatesDiehl, 2013). By exuding hydrophobic compounds, fungi tend toncrease hydrophobic soil organic matter that can avoid breakagef dry soil aggregates in the rewetting process and thus creat-ng more water stable aggregates (Six et al., 2004). This could ben line with more recent findings of Xu et al. (2015) who hadeported that AM fungi increased soil organic carbon which wasositively related to normalize mean weight diameter of aggre-ates. They suggested that increase in soil organic carbon by AMungi could be a mechanism through which fungi improve soil
tructure.
al inocula in the formation of soil aggregates.

4.3. Interaction between fungi and bacteria to improve soilaggregation and their stability

Fungi influence microbial communities in the soil rhizospherethrough many ways (as discussed above) and the interaction facili-tated by AM fungi leads to changes in the turnover and distributionof soil aggregates. However, these changes are arbitrated, and theprominence of these changes to soil aggregation and other medi-ated processes are poorly defined (Rillig et al., 2006). Fungi depositorganic compounds in the mycosphere through mycelium whichact as a substrate for the growth of microbes (bacteria and fungi).Bacteria isolated from fungal mycelium prove to be very impor-tant in formation of soil aggregates. According to Caesar-TonThatet al. (2013) Pseudomonas fluorescens and Stenotrophomonas mal-tophilia isolated from Agaricus lilaceps fruiting body binds soil morethan Bacillus sp. isolated from outside and inside of the fairy ring.Additionally, fungal activity can alter nature and extent of availabil-ity of pore spaces in the soil for the habitat of other surroundingmicrobes. This is in accordance with Gupta and Germida (2015)who reported that distribution of microbial diversity in soil is con-trolled by pore structure and aggregate hierarchy. Consequently,microbial biomass, bacteria and fungi community composition, aswell as their functional attributes vary within aggregate sizes (Chenet al., 2015; Gupta and Germida, 2015).

In addition to rhizospheres microbes, AM fungi can potentiallyinfluence soil aggregation by affecting plant communities, plantroots (individual host), and soil fauna such as earthworms, termitesor ants. These biota are considered to be key soil engineers (detailsabout these biotic interaction are not within the scope of this arti-cle) for pore size distribution and soil aggregation (Rillig et al., 2015;Bottinelli et al., 2015; Maaß et al., 2015). Fungal hyphae and plantroots binds and stabilize macroaggregates (>250 �m) in particular(Tisdall and Oades, 1982) whereas microaggregates (<250 �m) arestabilized by eternal binding agents like bacterial polysaccharides(Daynes et al., 2012); Table 3). Thus it is very likely that soil aggre-gation is the results of numerous interconnecting components orprocesses which are driven by different set of traits epitomized indifferent species (Rillig et al., 2015). Therefore, to reinstate the soilstructure in degraded soils, it would be unwise to rely only on one

as well as addition of organic fertilizers.

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which is not considered yet under field conditions. In above discus-sion, it had been highlighted that direct application and symbioticinteractions of bacterial and fungal inocula with crops and organic

6 M.I. Rashid et al. / Microbiol

. Organic amendments to reinstate soil fertility

Organic amendments such as animal manure (solid cattleanure and slurry), compost and crop residues could play an

mportant role in enhancing the fertility of degraded soil. Thesemendments increase the organic matter and thus influence theoil life by providing them a source of food. Enhancing soilrganic matter is the most important step to rehabilitate thetrongly degraded land. Since this parameter play a significanceole in increasing the capability of the ecosystem to support theore diverse and complex community composition, formation of

oil aggregates, maintenance of soil structure, fertility and waterolding capacity (Tiessen et al., 1994; Kononova, 2013). Rashidt al. (2014a) observed that continuous application of solid cat-le manure increased organic matter, N, pH, microbial biomass andoil fauna in sandy soil compared to that of slurry manure fertiliza-ion. Application of urban refuse increased soil microbial activitiess well as AM fungal diversity in degraded soil of semi-arid regiondel Mar Alguacil et al., 2009). In addition to these studies, use ofoultry manure and wheat straw in degraded soil of Himalayanegion increased organic matter content, hydraulic conductivity,ggregate stability, N, P, K, carbon sequestration and pH comparedo urea or unfertilized control (Khaliq and Abbasi, 2015). Combinepplication of solid cattle manure and chemical fertilizer increasedoil organic matter, N, microbial biomass and the crop productivitynd reduce the decreasing stock of soil carbon (Srinivasarao et al.,014). Tian et al. (2015) found that application of bio-solids withigh stable carbon and low carbon:N increase carbon sequestra-ion rate of crop residues than un-amended soil. They concludedhat use of such organic amendments in agricultural soil is a validpproach to transform them from current carbon-neutral status to aarbon sink. Moreover, application of bio-solids and vegetative yardompost increased fungal biomass and enzymatic activity in indus-rial degraded soil compared to un-amended control during the firstear of application however enzymatic activity was declined in theecond year (Carlson et al., 2015). Therefore, such findings couldestrict the lone use of organic amendments for the nutrient man-gement of degraded soil and may urge researcher to think of moreixed management option rather than simple solutions.

.1. Bacterial and fungal inocula to reinstate the fertility ofegraded land

Bacterial and fungal inocula play an important role in theestoration of degraded soil. Singh, (2014) reported that cyanobac-eria fix atmosphere N2 in degraded soils and release extracellularolysaccharides, which are metabolized by the associated soilicroorganisms. In addition, other bioactive compounds produced

y these bacteria positively influence soil fertility, decrease soilathogens and therefore improve crop growth (Singh, 2014). Bio-

ogical N2 fixing bacteria encourage the growth and persistencef other soil microbial groups in the rhizosphere by providing

(Seneviratne et al., 2008). Similarly bacteria exude extracel-ular polysaccharides that promote soil aggregations (Degens,997). Bacterial strains also mobilize the fixed or unavailable, K and Fe in the soil (discussed in various sections). In addi-ion to this, bacterial inocula also produce phyto-hormonesAuxin/Indole Acetic Acid) which improve plant defense againstarious pathogens (Lugtenberg and Kamilova, 2009; Ahemadnd Kibret, 2014; Goswami et al., 2015). These inocula alsoroduce aminocyclopropane-1-carboxylate deaminase that pro-otes the root elongation, shoot growth, and enhances rhizobial

odulation as well as N, P and K uptake in various cropsNadeem et al., 2009; Glick, 2012, 2015; Goswami et al., 2015).lant growth promoting bacteria induce systemic resistancend produce antifungal metabolites (HCN, phenazines, pyrrolni-

Research 183 (2016) 26–41

trin, 2,4-diacetylphloroglucinol, pyoluteorin, viscosinamide andtensin). Hence they act as biocontrol agent in various diseases andenvironmental stresses (Bhattacharyya and Jha, 2012; Goswamiet al., 2015). Ectomycorrhizal and AM fungi also increase the soilnutrient and water transport through soil exploration by theirhyphal network/pipelines and production of organic acids to mobi-lize the fixed nutrients (Andrade et al., 1997; Barea et al., 2005;Mortimer et al., 2008; Caesar-TonThat et al., 2013). AM Fungi canmobilize N, P, K, Fe and other nutrients in the soil and transfer thesenutrients to the host plants (Smith and Read, 2010) through translo-cation process by hyphal network (Fig. 2). AM fungi can reduce Nand P losses (Asghari and Cavagnaro, 2012) through leaching andN2O emission (Bender et al., 2015) and enhanced nutrient intercep-tion of AM fungi rooting systems. Due to these activities, microbialinocula drive nutrient cycling and at the same time also deter-mined whether these nutrients are made available to plants. Bydoing so, these microbial inocula can achieve satisfactory results inthe restoration of degraded soil. Seneviratne et al. (2011) observedthat application of biofilm based fertilizers developed from N2 fixerbacteria increased N2 fixation and soil organic carbon. Hence, thesefertilizers stimulated the ecosystem functioning and help in achiev-ing sustainable restoration of degraded agricultural soil within fewmonths in tropics. Microbial communities present in these biofilmbased fertilizers substantially enhanced the microbial biodiversitywhich leads to sustainability of agro-ecosystem and environment(Seneviratne et al., 2011).

5.2. Application of bacterial and fungal inocula with organicamendments to reinstate the fertility of degraded land

Few researchers use combination of bacteria or fungi inoculawith organic amendments to reinstate one or few parameters ofdegraded soil in controlled experiments and obtained promisingresults (Medina et al., 2004; Mengual et al., 2014a,b; Leifheit et al.,2015). For instance, Leifheit et al. (2015) used fungal inoculum withorganic residues to increase soil aggregation and their stability inpot experiment while Mengual et al., (2014a,b) found increase insoil P availability, total N and other microbiological and biochemicalparameters with co-application of bacterial inocula and compostedsugar beet in small field assay. Recently it was found that combinedeffect of bacterial and fungal inocula and cover crops increased Pmobilization and soil organic matter in subtropical red soils dur-ing a time duration of six months (Cui et al., 2015). They foundthat P. natatu tends to increase the soil organic matter by 5.2%(17.97 ± 1.02 vs. 17.07 ± 1.05 g kg−1) from control but it was not sta-tistically significant while inoculation of AM fungi further enhancedthis parameter by 5.4% (18.94 ± 1.03 vs. 17.97 ± 1.02, P > 0.05) fromP. natatu. Moreover, in this study moderately labile organic P wasalso increased from control (302.8 ± 4 vs. 272.5 ± 9.2, P = 0.05). Thisform of P strongly influence the phosphomonoesterase enzymeactivity (Cui et al., 2015). Hydrolytic enzymes released by soil inoc-ulants are main drivers of carbon, N and P cycling hence theyplay a key role in hastening the nutrients cycling in soils for plantgrowth (Burns et al., 2013). Thus, a combined application of organicamendments, cover crops, fungal and bacterial inocula could bea good approach for the sustainable restoration of degraded soil

fertilizers could be used as an emerging tool for restoring degradedlands. Therefore, adequate selection for the combined applicationof diverse communities of bacteria, fungi and organic fertilizerscould be a key to restore and reinstate the degraded ecosystems.

ogical

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.3. Gaps in current approaches and way forward to restore theegraded land

It is apparent from the above discussion that microbial inoc-la are one of the valuable bio-resources that could be helpful inestoring degraded lands. However, most of the researchers useone bacterium or fungal strain in their experiments that can par-ially result in the reported discrepancies at field scale (Table 4). Theeasons for lower response than co-inoculation could be that singleicrobial inoculum is not likely to be active as it faces competition

f resources from indigenous microorganisms in order to survive inoil environment (Singh, 2014, 2015). To make the inocula success-ul under field condition, it could be fascinating to test whether theombinations of ecologically diverse microbial strains, with akinunctions, and addition of organic fertilizers can meet the goal ofestoring the fertility of degraded lands. Such mixture of bacterialr fungal inocula may create synergistic effects (Singh, 2015) whilerganic manures can meet their nutrient demands to make themuccessful under field conditions. These associative interactionsould be successful and may play a crucial role in restoring the pro-uctivity of degraded soils. However, field experiments are lackingvidence to support these hypotheses. Singh (2015) proposed thatuccessful restoration of degraded soil using microbes required aombined knowledge on microbiology, ecology, biochemical mech-nisms and field engineering. Moreover, most of the soil functions.e. organic matter stabilization, decomposition, nutrient mobiliza-ion, translocation and mineralization, and aggregate formationnd stability are carried by microbes. To attain the sustainable pro-uctivity in agro-ecosystems, the aforementioned soil functionsave not been fully explored due to complex microbial diversity

n these soil ecosystems. Therefore, it is very important to furtherxplore unidentified microorganisms that can live in competitivenvironment under field conditions and help to increase the soilertility and productivity of degraded soils in order to meet thencreasing global food demand and at the same time environmentalustainability.

. Future considerations

Bacteria and fungi are integral part of soil microbial commu-ity. These microbes play a vital role in the restoration of degradedoils through fertility enhancement by affecting nutrients cycless well improvement in soil structure. Regardless of encouragingvidences on the application of microbial inocula for improvingutrient bio-availability and soil aggregation, still many aspectseed to be explored for further studies which are as follows:

. Many studies have revealed that the application of single bacte-rial or fungal inoculum or their co-inoculation to soil improvesits fertility and aggregation. In most cases, co-inoculation per-formed better than their sole/lone counterpart (Table 4) butthere are still certain aspects that require serious attention suchas evaluation of these approaches under field conditions. Major-ity of experimental studies are carried out in laboratory or inthe pots under controlled conditions, therefore performance oradaptability of these microorganisms under field condition maydiffer significantly. Under natural field conditions, both bioticand abiotic factors are not controlled and the competition forresources is higher thus affecting their performance.

. Application of organic fertilizers in combination with micro-bial inocula could have a potential to reinstate the fertility
and productivity of degraded land. However, adequate selec-tion of microbial inocula to enhance their synergistic effect hasnot gained much attention from the scientific community. Thisneeds to be further explored by the researchers.
Research 183 (2016) 26–41 37

3. To achieve sustainability in crop production, studies regardingmicrobial inocula should focus more on nutrient cycling (fix-ation, mobilization, translocation, leaching losses and gaseousemissions) rather than only single fate of the nutrient. There-fore the focus of future studies must be based on the processesto understand the influence of microbial inocula on nutrientcycling.

4. Bacterial and fungal inocula could be successfully employed inreinstating fertility of degraded soils. However, their applica-tions would consider the inherent limitations of these inoculaand figure out the best strains of both bacteria and AM fungi whocan establish a long-lasting association to improve the fertilityand structure of such soils.

7. Conclusions

In the coming decades, land degradation will be major threat tothe food security. Therefore most important issue is how to feed theincreasing population of the world where about 84% of agriculturalland per capita is declining and degrading due to its extensive use?Fungi and bacterial inocula and their combine use with organic fer-tilizers could be a promising approach for remediation of degradedsoil and would help to limit the extensive use of chemical fertilizers.Due to fixation, chelation, production of organic acid, siderophores,hydrophobins and glomalin protein, these microbes are capable ofenhancing nutrient bioavailability and improving soil aggregation.Hence they could be used in reinstating the fertility of degradedsoils. Understanding the mechanisms of microbial inocula in theprovision or mobilization of nutrients in degraded land is a keyfor their success in field applications. Although exact mechanismsthrough which bacteria and fungi achieve these benefits in suchsoils are not fully understood, however it is becoming clearer thatfew or all traits of these microbes can allow them to perform theirassociated functions. To this end, a better understanding on theinteraction of bacteria and fungi when applied under field condi-tions is required. The clarification of these mechanisms may helpin the development of innovative and cost effective managementpractices for improving the fertility and crop production capac-ity of degraded soils. Use of single inoculum or co-inoculation ofbacteria-bacteria, bacteria-fungi or fungi–fungi could not alwaysbe very fruitful for the reclamation of degraded soils. In fact, loneor dual strains with distinct functions are less active and couldnot survive in nutrient deficient soil environment due to compe-tition of resources for their survival. However, addition of organicfertilizer with co-inoculation of bacterial and fungal strains couldhave a potential for restoration of degraded soils because organicmatter can fulfill the nutrient demand while bacteria and fungican create synergistic effect for nutrient acquisition as well as soilaggregate formation and stabilization. Hence, inoculation of bacte-ria and fungi with organic fertilizers can reduce the excessive useof chemical fertilizers which are a serious concern for the farmers(especially those producing crops on moderately degraded soils)as well as on the environment. Therefore the central decree of thisstudy is to realize that for complete restoration of degraded soils, acombinatorial mixture of management practices is necessary. Thisincludes inoculation of soil biota (microbes and animal) in additionto organic fertilizers, plant roots and other associated factor likegrowing of cover crops.

Acknowledgments

This review was supported by the Ministry of Higher Education,Kingdom of Saudi Arabia, Centre of Excellence in EnvironmentalStudies, King Abdulaziz University, Jeddah, Kingdom of Saudi Ara-

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ia and Department of Environmental Sciences, COMSATS Institutef Information Technology, Vehari, Pakistan.

eferences

bou-el-Seoud, I.I., Abdel-Megeed, A., 2012. Impact of rock materials andbiofertilizations on P and K availability for maize (Zea Maize) under calcareoussoil conditions. Saudi J. of Biol. Sci. 19 (1), 55–63.

gerer, R., 2001. Exploration types of ectomycorrhizae. Mycorrhiza 11 (2),107–114.

hemad, M., Kibret, M., 2014. Mechanisms and applications of plant growthpromoting rhizobacteria: Current perspective. J. King Saud Univ.—Sci. 26 (1),1–20.

mbriz, E., Báez-Pérez, A., Sánchez-Yánez, J., Moutoglis, P., Villegas, J., 2010.Fraxinus–Glomus–Pisolithus symbiosis:plant growth and soil aggregationeffects. Pedobiologia 53 (6), 369–373.

mezketa, E., 1999. Soil aggregate stability: a review. J. Sustain. Agric. 14 (2-3),83–151.

ndrade, G., Mihara, K., Linderman, R., Bethlenfalvay, G., 1997. Bacteria fromrhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi.Plant Soil 192 (1), 71–79.

rmada, E., Portela, G., Roldán, A., Azcón, R., 2014. Combined use of beneficial soilmicroorganism and agrowaste residue to cope with plant water limitationunder semiarid conditions. Geoderma 232, 640–648.

sghari, H.R., Cavagnaro, T.R., 2012. Arbuscular mycorrhizas reduce nitrogen lossvia leaching. PLoS One 7 (1), e29825.

spiras, R., Allen, O., Harris, R., Chesters, G., 1971. The role of microorganisms inthe stabilization of soil aggregates. Soil Biol. Biochem. 3 (4), 347–353.

ai, Z.G., Dent, D.L., Olsson, L., Schaepman, M.E., 2008. Proxy global assessment ofland degradation. Soil Use Manag. 24 (3), 223–234.

area, J.-M., Pozo, M.J., Azcon, R., Azcon-Aguilar, C., 2005. Microbial co-operation inthe rhizosphere. J. Exp. Bot. 56 (417), 1761–1778.

ashan, Y., De-Bashan, L.E., 2010. Chapter two-how the plant growth-promotingbacterium Azospirillum promotes plant growth—a critical assessment. Adv.Agron. 108, 77–136.

ashan, Y., Holguin, G., De-Bashan, L.E., 2004. Azospirillum-plant relationships:physiological, molecular, agricultural, and environmental advances(1997–2003). Can. J. Microbiol. 50 (8), 521–577.

edini, S., Pellegrino, E., Avio, L., Pellegrini, S., Bazzoffi, P., Argese, E., Giovannetti,M., 2009. Changes in soil aggregation and glomalin-related soil protein contentas affected by the arbuscular mycorrhizal fungal species Glomus mosseae andGlomus intraradices. Soil Biol. Biochem. 41 (7), 1491–1496.

edini, S., Avio, L., Sbrana, C., Turrini, A., Migliorini, P., Vazzana, C., Giovannetti, M.,2013. Mycorrhizal activity and diversity in a long-term organic Mediterraneanagroecosystem. Biol. Fert. Soils 49 (7), 781–790.

ender, S.F., Conen, F., Van, der, H., eijden, M.G., 2015. Mycorrhizal effects onnutrient cycling, nutrient leaching and N 2 O production in experimentalgrassland. Soil Biol. Biochem. 80, 283–292.

hattacharjee, R.B., Singh, A., Mukhopadhyay, S., 2008. Use of nitrogen-fixingbacteria as biofertiliser for non-legumes: prospects and challenges. Appl.Microbiol. Biotechnol. 80 (2), 199–209.

hattacharyya, P.N., Jha, D.K., 2012. Plant growth-promoting rhizobacteria (PGPR):emergence in agriculture. World J. Microbiol. Biotechnol. 28 (4), 1327–1350.

ianciotto, V., Bandi, C., Minerdi, D., Sironi, M., Tichy, H.V., Bonfante, P., 1996. Anobligately endosymbiotic mycorrhizal fungus itself harbors obligatelyintracellular bacteria. Appl. Environ. Microbiol. 62 (8), 3005–3010.

iswas, J.C., Ladha, J.K., Dazzo, F.B., Yanni, Y.G., Rolfe, B.G., 2000. Rhizobialinoculation influences seedling vigor and yield of rice. Agron. J. 92 (5), 880–886.

laha, C.A.G., Schrank, I.S., 2003. An Azospirillum brasilense Tn5 mutant withmodified stress response and impaired in flocculation. Antonie VanLeeuwenhoek 83 (1), 35–43.

ona, E., Lingua, G., Manassero, P., Cantamessa, S., Marsano, F., Todeschini, V.,Copetta, A., D’Agostino, G., Massa, N., Avidano, L., 2014. AM fungi and PGPpseudomonads increase flowering, fruit production, and vitamin content instrawberry grown at low nitrogen and phosphorus levels. Mycorrhiza, 1–13.

orie, F., Rubio, R., Morales, A., 2008. Arbuscular mycorrhizal fungi and soilaggregation. J. Soil Sci. Plant Nutr. 8 (2), 9–18.

ottinelli, N., Jouquet, P., Capowiez, Y., Podwojewski, P., Grimaldi, M., Peng, X.,2015. Why is the influence of soil macrofauna on soil structure only consideredby soil ecologists? Soil Tillage Res. 146, 118–124.

oukhalfa, H.C., Crumbliss, A.L., 2002. Chemical aspects of siderophore mediatediron transport. Biometals 15 (4), 325–339.

ronick, C.J., Lal, R., 2005. Soil structure and management: a review. Geoderma124, 3–22, 1.

urns, R.G., DeForest, J.L., Marxsen, J., Sinsabaugh, R.L., Stromberger, M.E.,Wallenstein, M.D., Weintraub, M.N., Zoppini, A., 2013. Soil enzymes in achanging environment: current knowledge and future directions. Soil Biol.Biochem. 58, 216–234.

aesar-TonThat, A.J., 2002. Soil binding properties of mucilage produced by abasidiomycete fungus in a model system. Mycol. Res. 106 (08),
930–937.
aesar-TonThat, A.J., Espeland, E., Sainju, U.M., Lartey, R.T., Gaskin, J.F., 2013. Effectsof Agaricus lilaceps fairy rings on soil aggregation and microbial communitystructure in relation to growth stimulation of western wheatgrass (Pascopyrumsmithii) in eastern Montana rangeland. Microb. Ecol. 66 (1), 120–131.

Research 183 (2016) 26–41

Caesar-TonThat, T., Caesar, A., Gaskin, J., Sainju, U., Busscher, W., 2007. Taxonomicdiversity of predominant culturable bacteria associated with microaggregatesfrom two different agroecosystems and their ability to aggregate soil in vitro.Appl. Soil Ecol. 36 (1), 10–21.

Caesar-Tonthat, T.C., Stevens, W.B., Sainju, U.M., Caesar, A.J., West, M., Gaskin, J.F.,2014. Soil-aggregating bacterial community as affected by irrigation, tillage,and cropping system in the northern great plains. Soil Sci. 179 (1), 11–20.

Carlson, J., Saxena, J., Basta, N., Hundal, L., Busalacchi, D., Dick, R.P., 2015.Application of organic amendments to restore degraded soil: effects on soilmicrobial properties. Environ. Monit. Assess. 187 (3), 1–15.

Chaer, G.M., Resende, A.S., Campello, E.F.C., de, F., aria, S.M., Boddey, R.M., 2011.Nitrogen-fixing legume tree species for the reclamation of severely degradedlands in Brazil. Tree Physiol. 31 (2), 139–149.

Chang, C.-H.Y., Yang, S.-S., 2009. Thermo-tolerant phosphate-solubilizing microbesfor multi-functional biofertilizer preparation. Bioresour. Technol. 100 (4),1648–1658.

Chen, X., Li, Z., Liu, M., Jiang, C., Che, Y., 2015. Microbial community and functionaldiversity associated with different aggregate fractions of a paddy soil fertilizedwith organic manure and/or NPK fertilizer for 20 years. J. Soils Sediments 15(2), 292–301.

Chen, Y., Rekha, P., Arun, A., Shen, F., Lai, W.-A., Young, C., 2006. Phosphatesolubilizing bacteria from subtropical soil and their tricalcium phosphatesolubilizing abilities. Appl. Soil Ecol. 34 (1), 33–41.

Chenu, C., 1989. Influence of a fungal polysaccharide, scleroglucan, on claymicrostructures. Soil Biol. Biochem. 21 (2), 299–305.

Chenu, C., Stotzky, G., Huang, P., Bollag, J., Senesi, N., 2002. Interactions BetweenMicroorganisms and Soil Particles: An Overview. Interactions Between SoilParticles and Microorganisms: Impact on the Terrestrial Ecosystem IUPAC.John Wiley & Sons, Ltd., Manchester, UK, pp. 1–40.

Clark, R., Zobel, R., Zeto, S., 1999. Effects of mycorrhizal fungus isolates on mineralacquisition by Panicum virgatum in acidic soil. Mycorrhiza 9 (3), 167–176.

Cordell, D., Drangert, J.-O., White, S., 2009. The story of phosphorus: global foodsecurity and food for thought. Glob. Environ. Change 19 (2), 292–305.

Cui, H., Zhou, Y., Gu, Z., Zhu, H., Fu, S., Yao, Q., 2015. The combined effects of covercrops and symbiotic microbes on phosphatase gene and organic phosphorushydrolysis in subtropical orchard soils. Soil Biol. Biochem. 82, 119–126.

Dlamini, P., Chivenge, P., Manson, A., Chaplot, V., 2014. Land degradation impact onsoil organic carbon and nitrogen stocks of sub-tropical humid grasslands inSouth Africa. Geoderma 235, 372–381.

Dastager, S.G., Deepa, C., Pandey, A., 2010. Isolation and characterization of novelplant growth promoting Micrococcus sp NII-0909 and its interaction withcowpea. Plant Physiol. Biochem. 48 (12), 987–992.

Daynes, C.N., Zhang, N., Saleeba, J.A., McGee, P.A., 2012. Soil aggregates formedin vitro by saprotrophic Trichocomaceae have transient water-stability. SoilBiol. Biochem. 48, 151–161.

Daynes, C.N., Field, D.J., Saleeba, J.A., Cole, M.A., McGee, P.A., 2013. Developmentand stabilisation of soil structure via interactions between organic matter,arbuscular mycorrhizal fungi and plant roots. Soil Biol. Biochem. 57, 683–694.

Degens, B.P., 1997. Macro-aggregation of soils by biological bonding and bindingmechanisms and the factors affecting these: a review. Soil Res. 35 (3), 431–460.

del Mar Alguacil, M., Díaz-Pereira, E., Caravaca, F., Fernández, D.A., Roldán, A., 2009.Increased diversity of arbuscular mycorrhizal fungi in a long-term fieldexperiment via application of organic amendments to a semiarid degradedsoil. Appl. Environ. Microbiol. 75 (13), 4254–4263.

Demba Diallo, M., Willems, A., Vloemans, N., Cousin, S., Vandekerckhove, T.T., DeLajudie, P., Neyra, M., Vyverman, W., Gillis, M., van der Gucht, K., 2004.Polymerase chain reaction denaturing gradient gel electrophoresis analysis ofthe N2-fixing bacterial diversity in soil under Acacia tortilis ssp: raddiana andBalanites aegyptiaca in the dryland part of Senegal. Environ. Microbiol. 6 (4),400–415.

Diehl, D., 2013. Soil water repellency: dynamics of heterogeneous surfaces.Colloids Surfaces A: Physicochem. Eng. Aspects 432, 8–18.

Divito, G.A., Sadras, V.O., 2014. How do phosphorus, potassium and sulphur affectplant growth and biological nitrogen fixation in crop and pasture legumes? Ameta-analysis. Field Crops Res. 156, 161–171.

Dregne, H.E., 2002. Land Degradation in the Drylands. Arid Land Res. Manag. 16 (2),99–132.

Driver, J.D., Holben, W.E., Rillig, M.C., 2005. Characterization of glomalin as ahyphal wall component of arbuscular mycorrhizal fungi. Soil Biol. Biochem. 37(1), 101–106.

Duc, L., Noll, M., Meier, B.E., Bürgmann, H., Zeyer, J., 2009. High diversity ofdiazotrophs in the forefield of a receding alpine glacier. Microb. Ecol. 57 (1),179–190.

Egamberdiyeva, D., Höflich, G., 2004. Effect of plant growth-promoting bacteria ongrowth and nutrient uptake of cotton and pea in a semi-arid region ofUzbekistan. J. Arid Environ. 56 (2), 293–301.

FAO, 2009. Food and Agriculture Organization of the United Nations. How to feedthe World in 2050. www.fao.org/fileadmin/../How to Feed the World in 2050.pdf, website assessed 3 March 2015.

FAO, 2012. Food and Agriculture Organization of the United Nations. Current worldfertilizer trends and outlook to 2016. ftp://ftp.fao.org/ag/agp/docs/cwfto16.pdf,
website assessed 10 March 2015.
Figueiredo, M.V.B., Seldin, L., de Araujo, F.F., Mariano, R.L.R., 2011a. Plant growthpromoting rhizobacteria: fundamentals and applications. In: Plant Growth andHealth Promoting Bacteria. Springer, p. 21–43.

http://refhub.elsevier.com/S0944-5013(15)30028-8/sbref0005




































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































http://www.fao.org/fileadmin/../How_to_Feed_the_World_in_2050.pdf












http://ftp://ftp.fao.org/ag/agp/docs/cwfto16.pdf




























ogical

F

F

G

G

G

G

G

G

G

G

G

G

H

H

HI

I

I

I

J

J

K

K

K

K

K

K

K

K


igueiredo, M.V.B., Seldin, L., de Araujo, F.F., Mariano, R.L.R., 2011b. Plant growthpromoting rhizobacteria: fundamentals and applications. In: Maheshwari, D.K.(Ed.), Plant Growth and Health Promoting Bacteria, vol. 18. Springer, BerlinHeidelberg, pp. 21–43.

onte, S.J., Nesper, M., Hegglin, D., Velásquez, J.E., Ramirez, B., Rao, I.M., Bernasconi,S.M., Bünemann, E.K., Frossard, E., Oberson, A., 2014. Pasture degradationimpacts soil phosphorus storage via changes to aggregate-associated soilorganic matter in highly weathered tropical soils. Soil Biol. Biochem. 68,150–157.

alloway, J.N., Townsend, A.R., Erisman, J.W., Bekunda, M., Cai, Z., Freney, J.R.,Martinelli, L.A., Seitzinger, S.P., Sutton, M.A., 2008. Transformation of thenitrogen cycle: recent trends, questions, and potential solutions. Science 320(5878), 889–892.

lick, B.R., 1995. The enhancement of plant growth by free-living bacteria. Can. J.Microbiol. 41 (2), 109–117.

lick, B.R., 2012. Plant growth-promoting bacteria: mechanisms and applications.Scientifica 2012.

lick, B.R., 2015. Introduction to Plant Growth-promoting Bacteria. BeneficialPlant-Bacterial Interactions. Springer, pp. 1–28.

odfray, H.C.J., Beddington, J.R., Crute, I.R., Haddad, L., Lawrence, D., Muir, J.F.,Pretty, J., Robinson, S., Thomas, S.M., Toulmin, C., 2010. Food Security TheChallenge of Feeding 9 Billion People. Science 327 (5967), 812–818.

oldstein, A.H., 1994. Involvement of the quinoprotein glucose dehydrogenase inthe solubilization of exogenous phosphates by gram-negative bacteria. In:Phosphate in Microorganisms: Cellular and Molecular Biology. ASM Press,Washington, DC, pp. 197–203.

oswami, D., Patel, K., Parmar, S., Vaghela, H., Muley, N., Dhandhukia, P., Thakker,J.N., 2015. Elucidating multifaceted urease producing marine Pseudomonasaeruginosa BG as a cogent PGPR and bio-control agent. Plant Growth Regul. 75(1), 253–263.

raf, F., Frei, M., 2013. Soil aggregate stability related to soil density, root length,and mycorrhiza using site-specific Alnus incana and Melanogaster variegatus sl.Ecol. Eng. 57, 314–323.

upta, V.V.S.R., Germida, J.J., 2015. Soil aggregation: i nfluence on microbialbiomass and implications for biological processes. Soil Biol. Biochem. 80 (0),A3–A9.

yaneshwar, P., Kumar, G.N., Parekh, L., Poole, P., 2002. Role of soil microorganismsin improving P nutrition of plants. In: Food Security in Nutrient-StressedEnvironments: Exploiting Plants’ Genetic Capabilities. Springer, pp. 133–143.

alvorson, H., Keynan, A., Kornberg, H., 1990. Utilization of calcium phosphates formicrobial growth at alkaline pH. Soil Biol. Biochem. 22 (7), 887–890.

an, H., Lee, K., 2005. Phosphate and potassium solubilizing bacteria effect onmineral uptake, soil availability and growth of eggplant. Res. J. Agric. Biol. Sci.1, 176–180.

ubbell, D.H., Kidder, G., 2009. Biol. Nitrogen Fixation, 1–4.bijbijen, J., Urquiaga, S., Ismaili, M., Alves, B., Boddey, R., 1996. Effect of arbuscular

mycorrhizal fungi on growth, mineral nutrition and nitrogen fixation of threevarieties of common beans (Phaseolus vulgaris). New Phytol. 134 (2),353–360.

gual, J.M., Valverde, A., Cervantes, E., Velázquez, E., 2001. Phosphate-solubilizingbacteria as inoculants for agriculture: use of updated molecular techniques intheir study. Agronomie 21 (6-7), 561–568.

llmer, P., Schinner, F., 1992. Solubilization of inorganic phosphates bymicroorganisms isolated from forest soils. Soil Biol. Biochem. 24 (4), 389–395.

ndiragandhi, P., Anandham, R., Madhaiyan, M., Sa, T., 2008. Characterization ofplant growth–promoting traits of bacteria isolated from larval guts ofdiamondback moth Plutella xylostella (Lepidoptera: Plutellidae). Curr.Microbiol. 56 (4), 327–333.

astrow, J., Miller, R., Lussenhop, J., 1998. Contributions of interacting biologicalmechanisms to soil aggregate stabilization in restored prairie. Soil Biol.Biochem. 30 (7), 905–916.

ones, D.L., Oburger, E., 2011. Solubilization of phosphorus by soil microorganisms.In: Phosphorus in Action. Springer, pp. 169–198.

aschuk, G., Leffelaar, P.A., Giller, K.E., Alberton, O., Hungria, M., Kuyper, T.W.,2010. Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: ameta-analysis of potential photosynthate limitation of symbioses. Soil Biol.Biochem. 42 (1), 125–127.

emper, W.D., Rosenau, R.C., 1986. Methods of soil analysis. Part 1. In: Physical andMineralogical Methods. American Society of Agronomy, Inc.

haliq, A., Abbasi, M.K., 2015. Improvements in the physical and chemicalcharacteristics of degraded soils supplemented with organic-inorganicamendments in the Himalayan region of Kashmir, Pakistan. CATENA 126,209–219.

han, A.G., 2005. Role of soil microbes in the rhizospheres of plants growing ontrace metal contaminated soils in phytoremediation. J. Trace Ele. Med. Biol. 18(4), 355–364.

im, J., Rees, D.C., 1994. Nitrogenase and biological nitrogen fixation. Biochemistry33 (2), 389–397.

iss, T., Farkas, E., 1998. Metal-binding ability of desferrioxamine B. J. Incl.Phenom. Mol. Recognit. Chem. 32 (2–3), 385–403.

neip, C., Lockhart, C.P., Voß, C., Maier, U.G., 2007. Nitrogen fixation in
eukaryotes—new models for symbiosis C. BMC Evol. Biol. 7 (1), 55.
ohler-Milleret, R., Le, B., ayon, R.-C., Chenu, C., Gobat, J.-M., Boivin, P., 2013.Impact of two root systems, earthworms and mycorrhizae on the physicalproperties of an unstable silt loam Luvisol and plant production. Plant Soil 370(1–2), 251–265.

Research 183 (2016) 26–41 39

Kononova, M.M., 2013. Soil organic matter: Its nature, its role in soil formation andin soil fertility. Elsevier.

Kraaijvanger, R., Veldkamp, T., 2014. Grain productivity, fertilizer response andnutrient balance of farming systems in Tigray, Ethiopia: A multi-perspectiveview in relation to soil fertility degradation. Land Degrad. Dev. 26 (7), 701–710.

Kumar, V., Sarma, M., Saharan, K., Srivastava, R., Kumar, L., Sahai, V., Bisaria, V.,Sharma, A., 2012. Effect of formulated root endophytic fungus Piriformosporaindica and plant growth promoting rhizobacteria fluorescent pseudomonadsR62 and R81 on Vigna mungo. World J. Microbiol. Biotechnol. 28 (2), 595–603.

Larimer, A.L., Bever, J.D., Clay, K., 2010. The interactive effects of plant microbialsymbionts: a review and meta-analysis. Symbiosis 51 (2), 139–148.

Leifheit, E., Verbruggen, E., Rillig, M., 2015. Arbuscular mycorrhizal fungi reducedecomposition of woody plant litter while increasing soil aggregation. SoilBiol. Biochem. 81, 323–328.

Leifheit, E., Veresoglou, S., Lehmann, A., Morris, E.K., Rillig, M., 2014. Multiplefactors influence the role of arbuscular mycorrhizal fungi in soil aggregation—ameta-analysis. Plant Soil 374 (1–2), 523–537.

Lubbers, I.M., van, G., roenigen, K.J., Fonte, S.J., Six, J., Brussaard, L., van, G.,roenigen, J.W., 2013. Greenhouse-gas emissions from soils increased byearthworms. Nat. Clim. Change 3 (3), 187–194.

Lugtenberg, B., Kamilova, F., 2009. Plant-growth-promoting rhizobacteria. Ann.Rev. Microbiol. 63, 541–556.

Ma, J.F., 2005. Plant root responses to three abundant soil minerals: silicon,aluminum and iron. Crit. Rev. Plant Sci. 24 (4), 267–281.

Ma, Y., Rajkumar, M., Freitas, H., 2009. Inoculation of plant growth promotingbacterium Achromobacter xylosoxidans strain Ax10 for the improvement ofcopper phytoextraction by Brassica juncea. J. Environ. Manag. 90 (2), 831–837.

Maaß, S., Caruso, T., Rillig, M.C., 2015. Functional role of microarthropods in soilaggregation. Pedobiologia.

Machuca, A., Pereira, G., Aguiar, A., Milagres, A., 2007. Metal-chelating compoundsproduced by ectomycorrhizal fungi collected from pine plantations. Lett. Appl.Microbiol. 44 (1), 7–12.

Malik, K., Mirza, M., Hassan, U., Mehnaz, S., Rasul, G., Haurat, J., Bally, R., Normand,P., 2002. The role of plant-associated beneficial bacteria in rice-wheat croppingsystem. Biofertilisers in action Rural industries research and developmentCorporation. Canberra, 73–83.

Mansfeld-Giese, K., Larsen, J., Bødker, L., 2002. Bacterial populations associatedwith mycelium of the arbuscular mycorrhizal fungus Glomus intraradices.FEMS Microbiol. Ecol. 41 (2), 133–140.

Marshner, H., 1995. Mineral nutrition of higher plants. Academic Press, New YorkSan Diego, Ltd.

Martin, S., Mooney, S., Dickinson, M., West, H., 2012. The effects of simultaneousroot colonisation by three Glomus species on soil pore characteristics. Soil Biol.Biochem. 49, 167–173.

Medina, A., Roldán, A., Azcón, R., 2010. The effectiveness of arbuscular-mycorrhizalfungi and Aspergillus niger or Phanerochaete chrysosporium treated organicamendments from olive residues upon plant growth in a semi-arid degradedsoil. J. Environ. Manage. 91 (12), 2547–2553.

Medina, A., Vassileva, M., Caravaca, F., Roldán, A., Azcón, R., 2004. Improvement ofsoil characteristics and growth of Dorycnium pentaphyllum by amendmentwith agrowastes and inoculation with AM fungi and/or the yeast Yarowialipolytica. Chemosphere 56 (5), 449–456.

Meena, V.S., Maurya, B., Verma, J.P., 2014. Does a rhizospheric microorganismenhance K+ availability in agricultural soils? Microbiol. Res. 169 (5),337–347.

Mengual, C., Roldán, A., Caravaca, F., Schoebitz, M., 2014a. Advantages ofinoculation with immobilized rhizobacteria versus amendment with olive-millwaste in the afforestation of a semiarid area with Pinus halepensis Mill. Ecol.Eng. 73, 1–8.

Mengual, C., Schoebitz, M., Azcón, R., Roldán, A., 2014b. Microbial inoculants andorganic amendment improves plant establishment and soil rehabilitationunder semiarid conditions. J. Environ. Manage. 134, 1–7.

Miethke, M., Marahiel, M.A., 2007. Siderophore-based iron acquisition andpathogen control. Microbiol. Mol. Biol. Rev. 71 (3), 413–451.

Miller, R., Jastrow, J., 2000. Mycorrhizal fungi influence soil structure. Arbuscularmycorrhizas: physiology and function. Springer, pp. 3–18.

Miller, S.H., Browne, P., Prigent-Combaret, C., Combes-Meynet, E., Morrissey, J.P.,O’Gara, F., 2010. Biochemical and genomic comparison of inorganic phosphatesolubilization in Pseudomonas species. Environ. Microbiol. Rep. 2 (3), 403–411.

Minerdi, D., Fani, R., Gallo, R., Boarino, A., Bonfante, P., 2001. Nitrogen fixationgenes in an endosymbiotic Burkholderia strain. Appl. Environ. Microbiol. 67(2), 725–732.

Mirminachi, F., Zhang, A., Roehr, M., 2002. Citric acid fermentation and heavymetal ions: II. The action of elevated manganese ion concentrations. ActaBiotechnol. 22 (3-4), 375–382.

Montgomery, D.R., 2007. Soil erosion and agricultural sustainability. Proc. Natl.Acad. Sci. U. S. A. 104 (33), 13268–13272.

Mortimer, P., Pérez-Fernández, M., Valentine, A., 2008. The role of arbuscularmycorrhizal colonization in the carbon and nutrient economy of the tripartitesymbiosis with nodulated Phaseolus vulgaris. Soil Biol. Biochem. 40 (5),1019–1027.

Mrkovacki, N., Milic, V., 2001. Use of Azotobacter chroococcum as potentially usefulin agricultural application. Ann. Microbiol. 51 (2), 145–158.

Nadeem, S.M., Zahir, Z.A., Naveed, M., Arshad, M., 2009. Rhizobacteria containingACC-deaminase confer salt tolerance in maize grown on salt-affected fields.Can. J. Microbiol. 55 (11), 1302–1309.















































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































4 ogical

N

N

N

O

O

O

P

P

P

P

P

PPP

P

P

R

R

R

R

R

RR

R

R

R

R

R

R


asto, M.K., Alvarez-Clare, S., Lekberg, Y., Sullivan, B.W., Townsend, A.R., Cleveland,C.C., 2014. Interactions among nitrogen fixation and soil phosphorusacquisition strategies in lowland tropical rain forests. Ecol. Lett. 17 (10),1282–1289.

eubauer, U., Furrer, G., Kayser, A., Schulin, R., 2000. Siderophores, NTA, andcitrate: potential soil amendments to enhance heavy metal mobility inphytoremediation. Int. J. Phytorem. 2 (4), 353–368.

guyen, N., Bruns, T., 2015. The microbiome of pinus muricata ectomycorrhizae:community assemblages, fungal species effects, and burkholderia as importantbacteria in multipartnered symbioses. Microb. Ecol., 1–8.

ldeman L, Hakkeling Ru, Sombroek WG, 1990. World map of the status ofhuman-induced soil degradation: an explanatory note, International SoilReference and Information Centre.

rtiz, N., Armada, E., Duque, E., Roldán, A., Azcón, R., 2015. Contribution ofarbuscular mycorrhizal fungi and/or bacteria to enhancing plant droughttolerance under natural soil conditions: Effectiveness of autochthonous orallochthonous strains. J. Plant Physiol. 174, 87–96.

wen, D., Williams, A.P., Griffith, G.W., Withers, P.J.A., 2015. Use of commercialbio-inoculants to increase agricultural production through improvedphosphrous acquisition. Appl. Soil Ecol. 86 (0), 41–54.

armar, P., Sindhu, S., 2013. Potassium solubilization by rhizosphere bacteria:influence of nutritional and environmental conditions. J. Microbiol. Res. 3 (1),25–31.

aul, E., Kucey, R., 1981. Carbon flow in plant microbial associations. Science 213(4506), 473–474.

eng, S., Guo, T., Liu, G., 2013. The effects of arbuscular mycorrhizal hyphalnetworks on soil aggregations of purple soil in southwest China. Soil Biol.Biochem. 57, 411–417.

érès, G., Cluzeau, D., Menasseri, S., Soussana, J.-F., Bessler, H., Engels, C., Habekost,M., Gleixner, G., Weigelt, A., Weisser, W.W., 2013. Mechanisms linking plantcommunity properties to soil aggregate stability in an experimental grasslandplant diversity gradient. Plant Soil 373 (1-2), 285–299.

érez, C.A., Thomas, F.M., Silva, W.A., Segura, B., Gallardo, B., Armesto, J.J., 2014.Patterns of biological nitrogen fixation during 60 000 years of forestdevelopment on volcanic soils from south-central Chile. N. Z. J. Ecol. 38 (2),189–200.

ostgate, J.R., 1998. Nitrogen Fixation. Cambridge University Press, Cambridge, UK.ostgate, J.R., 1982. The fundamentals of nitrogen fixation, CUP Archive.rajapati, K., Sharma, M., Modi, H., 2012. Isolation of two potassium solubilizing

fungi from ceramic industry soils. Life Sci. Leaflets 5, 71–75.rakamhang, J., Tittabutr, P., Boonkerd, N., Teamtisong, K., Uchiumi, T., Abe, M.,

Teaumroong, N., 2015. Proposed some interactions at molecular level of PGPRcoinoculated with Bradyrhizobium diazoefficiens USDA110 and B. japonicumTHA6 on soybean symbiosis and its potential of field application. Appl. SoilEcol. 85, 38–49.

uppi, G., Azcón, R., Höflich, G., 1994. Management of positive interactions ofarbuscular mycorrhizal fungi with essential groups of soil microorganisms. In:Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and NaturalEcosystems. Springer, pp. 201–215.

ashid, M.I., de Goede, R.G., Brussaard, L., Lantinga, E.A., 2013. Home fieldadvantage of cattle manure decomposition affects the apparent nitrogenrecovery in production grasslands. Soil Biol. Biochem. 57, 320–326.

ashid, M.I., de Goede, R.G.M., Brussaard, L., Bloem, J., Lantinga, E.A., 2014a.Production-ecological modelling explains the difference between potential soilN mineralisation and actual herbage N uptake. Appl. Soil Ecol. 84, 83–92.

ashid, M.I., de Goede, R.G., Nunez, G.A.C., Brussaard, L., Lantinga, E.A., 2014b. SoilpH and earthworms affect herbage nitrogen recovery from solid cattle manurein production grassland. Soil Biol. Biochem. 68, 1–8.

eed, S.C., Cleveland, C.C., Townsend, A.R., 2007. Controls over leaf litter and soilnitrogen fixation in two lowland tropical rain forests. Biotropica 39 (5),585–592.

eed, S.C., Cleveland, C.C., Townsend, A.R., 2011. Functional ecology of free-livingnitrogen fixation: a contemporary perspective. Ann. Rev. Ecol. Evol. Syst. 42,489–512.

engel, Z., 2002. Breeding for better symbiosis. Plant Soil 245 (1), 147–162.iggs, P.J., Chelius, M.K., Iniguez, A.L., Kaeppler, S.M., Triplett, E.W., 2001. Enhanced

maize productivity by inoculation with diazotrophic bacteria. Funct. Plant Biol.28 (9), 829–836.

illig, M.C., Wright, S.F., Eviner, V.T., 2002. The role of arbuscular mycorrhizal fungiand glomalin in soil aggregation: comparing effects of five plant species. PlantSoil 238 (2), 325–333.

illig, M.C., Mummey, D.L., Ramsey, P.W., Klironomos, J.N., Gannon, J.E., 2006.Phylogeny of arbuscular mycorrhizal fungi predicts community composition ofsymbiosis-associated bacteria. FEMS Microbiol. Ecol. 57 (3), 389–395.

illig, M.C., Aguilar-Trigueros, C.A., Bergmann, J., Verbruggen, E., Veresoglou, S.D.,Lehmann, A., 2015. Plant root and mycorrhizal fungal traits for understandingsoil aggregation. New Phytol. 205 (4), 1385–1388.

odriguez, H., Gonzalez, T., Goire, I., Bashan, Y., 2004. Gluconic acid production andphosphate solubilization by the plant growth-promoting bacteriumAzospirillum spp. Naturwissenschaften 91 (11), 552–555.

odrııguez, H., Fraga, R., 1999. Phosphate solubilizing bacteria and their role in
plant growth promotion. Biotechnol. Adv. 17 (4), 319–339.
ömheld, V., Kirkby, E.A., 2010. Research on potassium in agriculture: needs andprospects. Plant Soil 335 (1–2), 155–180.

Research 183 (2016) 26–41

Sánchez-Díaz, M., Pardo, M., Antolin, M., Pena, J., Aguirreolea, J., 1990. Effect ofwater stress on photosynthetic activity in the Medicago–Rhizobium–Glomussymbiosis. Plant Sci. 71 (2), 215–221.

Schalk, I.J., Hannauer, M., Braud, A., 2011. New roles for bacterial siderophores inmetal transport and tolerance. Environ. Microbiol. 13 (11), 2844–2854.

Seneviratne, G., Zavahir, J., Bandara, W., Weerasekara, M., 2008. Fungal-bacterialbiofilms: their development for novel biotechnological applications. World J.Microbiol. Biotechnol. 24 (6), 739–743.

Seneviratne, G., Jayasekara, A., De, S., ilva, M., Abeysekera, U., 2011. Developedmicrobial biofilms can restore deteriorated conventional agricultural soils. SoilBiol. Biochem. 43 (5), 1059–1062.

Shah, G.M., Rashid, M.I., Shah, G.A., Groot, J.C.J., Lantinga, E.A., 2013. Mineralizationand herbage recovery of animal manure nitrogen after application to varioussoil types. Plant Soil 365 (1-2), 69–79.

Sharma, A., Johri, B., Sharma, A., Glick, B., 2003. Plant growth-promoting bacteriumPseudomonas sp: strain GRP 3 influences iron acquisition in mung bean (Vignaradiata L. Wilzeck). Soil Biol. Biochem. 35 (7), 887–894.

Shelobolina E., Roden E., Benzine J., Xiong M.Y., Using phyllosilicate-fe (ii)-oxidizingsoil bacteria to improve fe and K plant nutrition: Google Patents; 2014.

Sheng, X.F., He, L.Y., 2006. Solubilization of potassium-bearing minerals by awild-type strain of Bacillus edaphicus and its mutants and increasedpotassium uptake by wheat. Can. J. Microbiol. 52 (1), 66–72.

Sieverding, E., da Silva, G.A., Berndt, R., Oehl, F., 2014. Rhizoglomus, a new genus ofthe Glomeraceae. Mycotaxon 129 (2), 373–386.

Sinclair, T., Muchow, R., Bennett, J., Hammond, L., 1987. Relative sensitivity ofnitrogen and biomass accumulation to drought in field-grown soybean. Agron.J. 79 (6), 986–991.

Singh, J.S., 2014. Cyanobacteria: a vital bio-agent in eco-restoration of degradedlands and sustainable agriculture. Clim. Change Environ. Sustain. 2 (2),133–137.

Singh, J.S., 2015. Microbes. The chief ecological engineers in reinstatingequilibrium in degraded ecosystems. Agric. Ecosyst. Environ. 203, 80–82.

Six, J., Bossuyt, H., Degryze, S., Denef, K., 2004. A history of research on the linkbetween (micro) aggregates, soil biota, and soil organic matter dynamics. SoilTillage Res. 79 (1), 7–31.

Smil, V., 2000. Phosphorus in the environment: natural flows and humaninterferences. Annu. Rev. Energy Environ. 25 (1), 53–88.

Smith, S.E., Read, D.J., 2010. Mycorrhizal Symbiosis. Academic press, Cambrige.Song, X., Liu, M., Wu, D., Griffiths, B.S., Jiao, J., Li, H., Hu, F., 2015. Interaction

matters: Synergy between vermicompost and PGPR agents improves soilquality, crop quality and crop yield in the field. Appl. Soil Ecol. 89, 25–34.

Sparks, D.L., Huang, P.M., 1985. Physical Chemistry of Soil Potassium. In: Munson,R.D. (Ed.), Potassium in Agriculture American Society of Agronomy, CropScience Society of America, Soil Science Society of America Madison, WI,201–276.

Sprent J., Sutherland M., De Faria S., Structure and function of nodules from woodylegumes. 1989.

Srinivasarao, C., Venkateswarlu, B., Lal, R., Singh, A., Kundu, S., Vittal, K., Patel, J.,Patel, M., 2014. Long-term manuring and fertilizer effects on depletion of soilorganic carbon stocks under pearl millet-cluster bean-castor rotation inwestern india. Land Degr. Dev. 25 (2), 173–183.

Stacey, G., 2007. The Rhizobium-legume nitrogen-fixing symbiosis. In: Biology ofthe Nitrogen Cycle. Elsevier, London, pp. 147.

Sun, T., Chen, Q., Chen, Y., Cruse, R., Li, X., Song, C., Kravchenko, Y., Zhang, X., 2014.A novel soil wetting technique for measuring wet stable aggregates. SoilTillage Res. 141, 19–24.

Tang, J., Mo, Y., Zhang, J., Zhang, R., 2011. Influence of biological aggregating agentsassociated with microbial population on soil aggregate stability. Appl. Soil Ecol.47 (3), 153–159.

Tao, G.-C., Tian, S.-J., Cai, M.-Y., Guang-Hui, X., 2008. Phosphate-solubilizingand-mineralizing abilities of bacteria isolated from soils. Pedosphere 18 (4),515–523.

Tian, G., Chiu, C.-Y., Franzluebbers, A.J., Oladeji, O.O., Granato, T.C., Cox, A.E., 2015.Biosolids amendment dramatically increases sequestration of cropresidue-carbon in agricultural soils in western Illinois. Appl. Soil Ecol. 85,86–93.

Tiessen, H., Cuevas, E., Chacon, P., 1994. The role of soil organic matter insustaining soil fertility. Nature 371 (6500), 783–785.

Tilman, D., Balzer, C., Hill, J., Befort, B.L., 2011. Global food demand and thesustainable intensification of agriculture. Proc. Natl. Acad. Sci. U. S. A. 108 (50),20260–20264.

Tisdall, J., 1994. Possible role of soil microorganisms in aggregation in soils. PlantSoil 159 (1), 115–121.

Tisdall, J., Oades, J.M., 1982. Organic matter and water-stable aggregates in soils. J.Soil Sci. 33 (2), 141–163.

Tytova, L.V., Brovko, I.S., Kizilova, A.K., Kravchenko, I.K., Iutynska, G.A., 2013. Effectof complex microbial inoculants on the number and diversity of rhizosphericmicroorganisms and the yield of soybean. Int. J. 4 (3), 267–274.

Uroz, S., Calvaruso, C., Turpault, M.-P., Frey-Klett, P., 2009. Mineral weathering bybacteria: ecology, actors and mechanisms. Trends Microbiol. 17 (8), 378–387.

Utuk, I.O., Daniel, E.E., 2015. land degradation: a threat to food security: a global
assessment. J. Environ. Earth Sci. 5 (8), 13–21.
van der Heijden, M.G., Bardgett, R.D., Van Straalen, N.M., 2008. The unseenmajority: soil microbes as drivers of plant diversity and productivity interrestrial ecosystems. Ecol. Lett. 11 (3), 296–310.




















































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































































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an Lynden, L., Odeman, G., 1998. The Assessment of the Status of Human-inducedSoil Degradation in South and Southeast Asia. ISRIC.

an Vuuren, D.P., Bouwman, A., Beusen, A., 2010. Phosphorus demand for the1970–2100 period: a scenario analysis of resource depletion. Glob. Environ.Change 20 (3), 428–439.

andenberghe, L.P., Soccol, C.R., Pandey, A., Lebeault, J.-M., 1999. Microbialproduction of citric acid. Braz. Arch. Biol. Technol. 42 (3), 263–276.

ansuyt, G., Robin, A., Briat, J.-F., Curie, C., Lemanceau, P., 2007. Iron acquisitionfrom Fe-pyoverdine by Arabidopsis thaliana. Mol. Plant Microbe Interact. 20(4), 441–447.

eresoglou, S.D., Chen, B., Rillig, M.C., 2012. Arbuscular mycorrhiza and soilnitrogen cycling. Soil Biol. Biochem. 46, 53–62.

ang, J., Zhao, F.-J., Meharg, A.A., Raab, A., Feldmann, J., McGrath, S.P., 2002.Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake kinetics,interactions with phosphate, and arsenic speciation. Plant Physiol. 130 (3),1552–1561.

right, S.F., Upadhyaya, A., 1996. Extraction of an abundant and unusual protein
from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi.Soil Sci. 161 (9), 575–586.
u, Q.-S., Cao, M.-Q., Zou, Y.-N., He, X.-h, 2014. Direct and indirect effects ofglomalin, mycorrhizal hyphae, and roots on aggregate stability in rhizosphereof trifoliate orange. Sci. Repo. 4.

Research 183 (2016) 26–41 41

Wu, S., Cao, Z., Li, Z., Cheung, K., Wong, M., 2005. Effects of biofertilizer containingN-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial.Geoderma 125 (1), 155–166.

Xu, P., Liang, L.Z., Dong, X.Y., Shen, R.F., 2015. Effect of arbuscular mycorrhizal fungion aggregate stability of a clay soil inoculating with two different host plants.Acta Agric. Scand., Section B—Soil Plant Sci. 65 (1), 23–29.

Yadav, J., Verma, J.P., Jaiswal, D.K., Kumar, A., 2014. Evaluation of PGPR anddifferent concentration of phosphorus level on plant growth, yield andnutrient content of rice (Oryza sativa). Ecol. Eng. 62, 123–128.

Zadorova, T., Jaksík, O., Kodesová, R., Penízek, V., 2011. Influence of terrainattributes and soil properties on soil aggregate stability. Soil Water Res. 6 (3),111.

Zarjani, J.K., Aliasgharzad, N., Oustan, S., Emadi, M., Ahmadi, A., 2013. Isolation andcharacterization of potassium solubilizing bacteria in some Iranian soils. Arch.Agron. Soil Sci. 59 (12), 1713–1723.

Zhang, L., Fan, J., Ding, X., He, X., Zhang, F., Feng, G., 2014. Hyphosphereinteractions between an arbuscular mycorrhizal fungus and a phosphate
solubilizing bacterium promote phytate mineralization in soil. Soil Biol.Biochem. 74, 177–183.
Zheng, W., Morris, E.K., Rillig, M.C., 2014. Ectomycorrhizal fungi in association withPinus sylvestris seedlings promote soil aggregation and soil water repellency.Soil Biol. Biochem. 78, 326–331.




























































































































































































































































































































bacteria and fungi can contribute to nutrients bioavailability and … · 2 ﬁxation in degraded...

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