Bacteria and Fungi Can Contribute to Nutrients Bioavailability And

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Microbiological Research 183 (2016) 26–41

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Microbiological Research

j ournal homepage: www.elsevier.com/locate/micres

Bacteria and fungi can contribute to nutrients bioavailability and

aggregate formation in degraded soils

a,d,∗ a e

Muhammad Imtiaz Rashid , Liyakat Hamid Mujawar , Tanvir Shahzad ,

a,b a,c a

Talal Almeelbi , Iqbal M.I. Ismail , Mohammad Oves

Center of Excellence in Environmental Studies, King Abdulaziz University, P.O Box 80216, Jeddah 21589, Saudi Arabia

Department of Environmental Sciences, King Abdulaziz University, Jeddah 2158, Saudi Arabia

Department of Chemistry, King Abdulaziz University, Jeddah 2158, Saudi Arabia

Department of Environmental Sciences, COMSATS Institute of Information Technology, 61100, Vehari, Pakistan

Department of Environmental Sciences & Engineering, Government College University, 38000, Faisalabad, Pakistan

r t i c l e i n f o a b s t r a c t

Article history: Intensive agricultural practices and cultivation of exhaustive crops has deteriorated soil fertility and its

Received 13 October 2015

quality in agroecosystems. According to an estimate, such practices will convert 30% of the total world

Received in revised form

cultivated soil into degraded land by 2020. Soil structure and fertility loss are one of the main causes

16 November 2015

of soil degradation. They are also considered as a major threat to crop production and food security for

Accepted 21 November 2015

future generations. Implementing safe and environmental friendly technology would be viable solution

Available online 25 November 2015

for achieving sustainable restoration of degraded soils. Bacterial and fungal inocula have a potential to

reinstate the fertility of degraded land through various processes. These microorganisms increase the

Keywords:

nutrient bioavailability through nitrogen ﬁxation and mobilization of key nutrients (phosphorus, potas-

Degraded land

sium and iron) to the crop plants while remediate soil structure by improving its aggregation and stability.

Food security

Microbial inocula Success rate of such inocula under ﬁeld conditions depends on their antagonistic or synergistic interac-

Nutrient bioavailability tion with indigenous microbes or their inoculation with organic fertilizers. Co-inoculation of bacteria and

Soil fertility fungi with or without organic fertilizer are more beneﬁcial for reinstating the soil fertility and organic

Siderophores

matter content than single inoculum. Such factors are of great importance when considering bacteria

Soil aggregation

and 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 of

degraded soil and assist them in reducing the negative impact of artiﬁcial fertilizers on our environment.

Contents

1. Introduction ...... 27

2. Reinstating fertility of degraded soils ...... 28

2.1. Microbial inocula and soil nutrient bioavailability ...... 29

2.1.1. Nitrogen ﬁxation ...... 29

2.1.2. N2 ﬁxation in degraded land ...... 29

3. Mechanisms used by microbes to reinstate the fertility of degraded soils ...... 29

3.1. Fungi and N2 ﬁxation ...... 29

3.1.1. How do fungi inﬂuence N2 ﬁxation? ...... 30

3.2. Phosphorus mobilization...... 30

3.3. Potassium...... 31

∗

Corresponding author at: King Abdulaziz University, Center of Excellence in Environmental Studies, P.O Box 80216, Jeddah 21589, Saudi Arabia. Fax: +966 12 6951674.

E-mail addresses: [email protected] (M.I. Rashid), [email protected] (M. Oves).

http://dx.doi.org/10.1016/j.micres.2015.11.007

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

3.3.1. Fungi and K mobilization ...... 31

3.3.2. How do bacterial and fungal inocula increase K mobilization? ...... 31

3.4. Role of bacteria in Fe mobilization ...... 31

3.5. Interaction between bacteria and fungi inocula to improve nutrient bioavailability in soil ...... 33

4. Soil structure ...... 33

4.1. Bacteria and soil aggregation ...... 34

4.2. Fungi and soil aggregation ...... 34

4.2.1. How do fungi inﬂuence soil aggregation? Mechanism ...... 35

4.3. Interaction between fungi and bacteria to improve soil aggregation and their stability ...... 35

5. Organic amendments to reinstate soil fertility ...... 36

5.1. Bacterial and fungal inocula to reinstate the fertility of degraded land ...... 36

5.2. Application of bacterial and fungal inocula with organic amendments to reinstate the fertility of degraded land ...... 36

5.3. Gaps in current approaches and way forward to restore the degraded land...... 37

6. Future considerations ...... 37

7. Conclusions ...... 37

Acknowledgments ...... 37

References ...... 38

1. Introduction in many parts of the world. Therefore, efforts are necessary to ﬁg-

ure out alternative, innovative, environmental friendly options to

The global human population is increasing continuously, that reduce the use of costly and non-environmental friendly chem-

has propelled up to 7 billion at present (Godfray et al., 2010; Glick, ical fertilizers. In this context, microbes (i.e., bacteria and fungi)

2015). At this projected growth rate, the world population will rise naturally occurring in soil or supplied as bio-fertilizers, could rep-

to about 9.5 billion by 2050, thus exerting immense pressure on resent a promising approach to increase nutrients bioavailability

food supplies (Glick, 2015). According to FAO (2009), the global food and improve soil structure.

demands in coming decades will raise by 70%, which will enhance Bacterial and fungal inocula and organic amendments could

the need of intensively growing agricultural crops (Godfray et al., be considered as a potential option to incorporate in crop inte-

2010; Tilman et al., 2011). To encounter this issue, soils are culti- grated nutrient management strategy of degraded soils (Medina

vated with extractive crops which depleted the nutrient reserves et al., 2010; Chaer et al., 2011). Introduction of these inoc-

that had led to negative balance of nutrients and soil degrada- ula can exploit, translocate, mineralize and mobilize soil P, K,

tion (van Lynden and Odeman, 1998; Kraaijvanger and Veldkamp, Fe reserves, increase organic matter or ﬁx N from the atmo-

2014). This can be deﬁned as physio-chemical and biological deteri- sphere (Figueiredo et al., 2011b; Ahemad and Kibret, 2014;

oration of soil environment through anthropogenic activity leading Leifheit et al., 2014; Nguyen and Bruns, 2015; Owen et al., 2015).

to a serious decline in soil productivity and fertility (Dregne, 2002). According to van der Heijden et al. (2008), arbuscular mycorrhizal

The other dominant form of soil degradation are erosion and salin- (AM) fungi and biological N ﬁxing bacteria annually contribute

ity, where the causative factors for former type include improper 5–20% to the total N demand of grassland and savannah. The contri-

agricultural practices, deforestation and overgrazing (van Lynden bution of AM fungi to temperate and boreal forests is 80% whereas

and Odeman, 1998, Fig. 1). These practices degrade 38% of the total P acquired by plants through bacteria and fungi was 75%.

world agricultural land, 21% permanent pasture and 18% forests The basic mechanisms through which bacteria and fungi promote

and woodlands (Oldeman et al., 1990; Utuk and Daniel, 2015). Of nutrients bioavailability include N ﬁxation, P, K and Fe mobiliza-

the total degraded cropland, pasture and woodland, Oldeman et al. tion through production of organic acids and siderophores (Fig. 1).

(1990) categorized as lightly (9%), moderately (10%) and strongly In addition to this, organo-polysaccharides and proteins (golma-

(4%) degraded soils. Light and moderately degraded soils are suit- lin, mucilages and hydrophobins) are also produced that help to

able for local farming with reduced agricultural functions. A large promote soil aggregate stability (Fig. 1) (Mortimer et al., 2008;

decline in productivity of such soils and their restoration is possi- Glick, 2012; Caesar-Tonthat et al., 2014; Nguyen and Bruns, 2015;

ble with changes in farm management practices whereas severely Owen et al., 2015). These processes are carried out by bacteria, and

degraded soil virtually lose their productivity and their original AM fungi. Later group of microbes form a symbiotic association

biotic functionality (Oldeman et al., 1990; Utuk and Daniel, 2015). with legume roots infected by N ﬁxing bacteria that increase P,

In former soils, removal of organic matter and nutrient rich layer of micro and other macronutrients for plant uptake as well as miti-

soil proﬁle causes nutrient depletion, the loss of soil fertility, struc- gate the effect of water and salt stress (Sánchez-Díaz et al., 1990;

ture and water holding capacity (Montgomery, 2007). Production Nadeem et al., 2009). Free-living and symbiotic bacteria enhance

of agricultural crops on such soil strongly depends on the nutrient plant growth by providing N through atmospheric N2 ﬁxation and

availability and good soil structure for supporting plant growth. produce (phyto)-hormone (auxins, cytokinins and gibberellins) in

Nitrogen (N), phosphorus (P), potassium (K) and iron (Fe) are addition to anti-microbial molecules to protect the crops from dis-

key nutrients that play a major role in crop production on degraded eases (Khan, 2005).

soils. As most of the soils in the world are known to be deﬁcient in In the past, agriculturists had immensely practiced the appli-

aforementioned nutrients, there will be a great demand of chemi- cation of earthworms and organic fertilizers to improve the soil

cal fertilizers to fulﬁll nutrients deﬁciency. According to FAO (2012), fertility (Rashid et al., 2013; Shah et al., 2013; Rashid et al., 2014b,

by the end of 2016 the global requirement of chemical fertilizers 2014a). Both practices prove to be beneﬁcial for soil nutrient

(N, P, K and other macronutrients) is expected to reach 194 mil- management of agroecosystems. However, earthworm enhanced

lion tons. Manufacturing of the chemical fertilizers to meet this greenhouse gaseous emissions (Lubbers et al., 2013), and their

demand requires a huge amount of nonrenewable resources such as successful functioning was achieved at an expense of maintain-

energy in the form of oil and natural gas. In addition, excessive use ing their healthy population in soil. Such high maintenance costs

of chemical fertilizers has also contributed to soil and air pollution would directly affect the price index of the crops. Another possibil-

(greenhouse gaseous emissions) as well as water eutrophication 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

Fig. 1. Mechanisms used by bacteria and fungi to improve soil organic matter (SOM), nutrient availability and aggregation.

microorganisms such as bacteria and fungi. These microorganisms fungal-mediated soil nutrient enhancement and aggregation is still

are omnipresent and found in various components of earth such as underdeveloped. Novel ﬁeld-based studies and experiments under

water and soil. controlled conditions need to be planned to lend better accuracy in

Bacteria and fungi are also known to improve soil struc- the understanding of microbial inﬂuenced soil fertility and struc-

ture by promoting the formation of soil aggregates and pores tural attributes. The main objective of present review is to highlight

within (Degens, 1997; Miller and Jastrow, 2000). Fungal cells and discuss current knowledge on the mechanisms used by bacte-

release mucilaginous exudates which are mainly composed of ria and fungi inocula to inﬂuence soil nutrient bioavailability (N, P,

extracellular surface polysaccharides; cell wall polysaccharides K and Fe; other nutrient are not in the scope of this review) and

and somatic or intracellular polysaccharides located inside the aggregation. We will discuss the effectiveness of these microbes

cytoplasmic membrane. Extracellular polysaccharides are mainly when inoculated solely, as co-inoculant or in combination with

responsible for the formation of aggregates, which are beneﬁcial organic fertilizer in improving fertility and aggregation stability of

for improving porosity and aeration in soil. Moreover, bacteria degraded soils.

release exopolysaccharides that form organo-mineral complexes

which help to bind soil particles into aggregates (Degens, 1997).

Experimentally it has been proved that soil structure is not only 2. Reinstating fertility of degraded soils

inﬂuenced by the mineral constituents of the soil but also by the

presence of micro-organisms in pores (Gupta and Germida, 2015). Land degradation is a worldwide problem caused by number

On the other hand, exudates from bacteria, fungi, decomposed cells of human induced processes that result in loss of soil fertility and

as well as plant and animal residues especially in soils managed by productivity. The major causes of the land degradation includes

organic inputs are also responsible to boost the soil organic matter deforestation, improper agricultural practices, (intensive cultiva-

which in turn improve the soil structure, function and quality. tion, unbalanced fertilization, poor quality irrigation and chemical

Reconnoitering the mechanisms of bacterial and fungal inoc- inputs in the form of fertilizers or pesticides) and industrializa-

ula together with organic fertilizer could be very valuable tool tion (Dregne 2002). Moreover, Dlamini et al. (2014) have associated

for improving soil fertility (Song et al., 2015) and aggregation. land degradation with decrease in soil organic carbon and N stocks.

Such strategy may help in planning a chemical fertilizer-free, envi- According to estimation by Bai et al. (2008), about 40% of the world

ronmental friendly integrated soil nutrient management to meet agricultural soils are seriously degraded whereas 24% area of the

global food demand which may further help in reinstating the productive soils is still under continuous degradation. This requires

fertility of degraded soil. In this regard, various aspects of the special attention to ﬁgure out alternative and sustainable nutrient

bacterial and fungal-mediated soil nutrient acquisition processes management techniques that can reinstate the fertility of such soils.

and aggregate formation have also been recognized. Co-inoculation Integrated management of microbial inocula and organic fertilizers

of bacteria and fungi with organic amendments could be an elo- could be an alternative option which needs to be explored in future

quent approach for sustainable management of soil fertility and studies. In the following sections, few approaches for restoring the

crop production (Minerdi et al., 2001; Rillig et al., 2002; Mortimer fertility of degraded soils are discussed. However, the limited focus

et al., 2008; Caesar-Tonthat et al., 2014) in strongly degraded soil. of following discussion will not provide complete guidelines for

In order to avail maximum beneﬁts from such approaches, there attaining sustainable restoration of degraded soil, but it describes

are still many undeveloped facets that need to be explored in few essential management options that could be important to con-

future studies. The mechanistic understanding of bacterial and sider in this regard.

M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41 29

2.1. Microbial inocula and soil nutrient bioavailability tion of microbial N ﬁxation (Postgate, 1998) is shown in following

equation.

Various species of bacteria and fungi play a key role in improv-

+ −

+ + + → + + +

ing soil fertility. These microbes increase organic matter that boosts N2 8 H 8e 16MgATP 2NH3 H2 16MgADP 16Pi

the availability of N, P, K and Fe in soil (Egamberdiyeva and Höﬂich,

2004; Caesar-Tonthat et al., 2014; Leifheit et al., 2015). Additionally,

they also produce organic acids for the mobilization of nutrients

2.1.2. N2 ﬁxation in degraded land

and facilitate their plant uptake from the rhizosphere. The simi-

Phosphorus (P), potassium (K) and sulphur are generally lim-

larities or differences in bacteria and fungi to inﬂuence nutrient

ited in degraded soils. Under nutrient limited conditions, these

bioavailability and aggregate formation are discussed in Table 1.

nutrients affect the N2 ﬁxation by reducing the growth of N-ﬁxing

In this manner, the application of chemical fertilizers in agro-

bacteria, nodule formation and functioning, as well as affecting

ecosystems can be greatly reduced (Figueiredo et al., 2011a). Hence,

host plant growth. Meta-analysis study of Divito and Sadras (2014)

application of microbial inocula would not only help the farmers to

conﬁrmed that nodule production, activity and their number are

reduce the additional costs of chemical fertilizers but also assist

limited more than plant shoot biomass in response to the deﬁciency

in obtaining high crop yield. Most of the processes through which

of P, K and sulphur. Moreover, P limitation in soil decreases the

microbial inocula promote soil fertility are not fully understood,

activity of nitrogenase enzyme in N-ﬁxing bacteria, because both

however it is believed that microbes use several direct and indirect

autotrophic and heterotrophic bacteria require high ATP for cellu-

mechanisms (Glick, 2012). These are highlighted and reviewed in

lar N2 ﬁxation (Reed et al., 2007, 2011; Pérez et al., 2014). Similar to

forthcoming sections.

nutrient deﬁciency, soil moisture is another major factor that inﬂu-

ences nodule formation or retardation of nodule growth. Water

2.1.1. Nitrogen ﬁxation

availability in soil is related to water holding capacity which is very

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

low in degraded soil (Montgomery, 2007). According to Sinclair

their growth and metabolism. It is often lost through leaching or

et al. (1987) water limiting conditions severely affect nodule for-

emission thus limiting its availability in most of the cultivated

mation in soybean crop. Thus in degraded soils, N2 ﬁxation and

soils. Although N is present abundantly in atmosphere in the form

other related functions (decomposition, mineralization, enzymes

of diatomic (N2) molecule, but its structure makes N2 molecule

or organic production) of microbes are severely affected due to loss

inert. However, reduction of N2 molecule into N is a complex pro-

of fertility and water holding capacity. Soil microbes adapt vari-

cess which requires input of huge amount of energy (Postgate,

ous strategies to cope with such deﬁciencies. These strategies are

1982). Prokaryotic microorganisms known as diazotrophs ﬁx atmo-

discussed in the forthcoming sections.

spheric N2 in the form of ammonia (NH3) through their normal

metabolic process (Riggs et al., 2001; Galloway et al., 2008). These

3. Mechanisms used by microbes to reinstate the fertility of

microbes are free living organisms present in the bulk soil (Reed

degraded soils

et al., 2011) that mainly includes Cyanobacteria, Proteobacteria,

Archaea, and Firmicutes (Demba Diallo et al., 2004; Duc et al., 2009).

3.1. Fungi and N ﬁxation

Some of these organisms (Azotobacter and Azoarcus genera) are 2

also present at comparable densities in the rhizosphere and bulk

In light and moderately degraded soils, AM fungi play an impor-

soil. However, there are other bacteria from genera Herbaspirillum

tant role in N ﬁxation by providing favorable environment for the

and Azospirillum that colonize only in the rhizosphere (Mrkovacki 2

bacteria to infect plant root. As indicated by Puppi et al. (1994) and

and Milic, 2001; Malik et al., 2002; Bashan et al., 2004; Bashan

Nasto et al. (2014), AM colonization can fulﬁll high demands of P

and De-Bashan, 2010). Rhizobia has the capability to infect roots

required by nitrogenase enzymes for N ﬁxation when inoculated

and induce the formation of root nodules (Stacey, 2007). There- 2

with N ﬁxer rather than non-N ﬁxer to increase the growth of

fore in the ﬁeld of N ﬁxation, most of the researchers specially 2 2

host plant. Many studies reported that co-inoculation of bacteria or

focus on rhizobium-legume symbiosis due to higher impact on

legumes with AM fungi increased N ﬁxation ability of legumes or

primary productivity of the agricultural ecosystem (Rengel, 2002). 2

trees (Ibijbijen et al., 1996; Bona et al., 2014). However, this increase

The establishment of this association results in the formation of

in N ﬁxation ability does not necessarily mean that growth and

highly specialized organ called ‘nodules’ that are formed on the 2

productivity of host plants will increase. Meta analyses studies by

intracellular root of symbionts, on which bacteria colonize. Such

Larimer et al. (2010) and Kaschuk et al. (2010) have shown that

bacteria mainly belong to the family Rhizobiaceae that develop a

co-inoculation of AM fungi with rhizobia or free living N-ﬁxing

highly speciﬁc interaction with the infected root. This interaction

bacteria resulted in a non-additive effect on the growth of host

consists of several stages which involves the exchange of complex

plant. However, plant growth responses were positive when AM

signals between the bacterium and plant (Sprent et al., 1989). Bac-

fungi or N ﬁxer were inoculated alone. Extra-radical hyphae of AM

teria ﬁx N2 through a complex enzyme system called nitrogenase 2

seem to have ability to ﬁx atmospheric N through N-ﬁxing bacteria

(Kim and Rees, 1994) and this enzyme system exists as two sep- 2

present in mycelia. According to Bianciotto et al. (1996) and Minerdi

arable components; (1) dinitrogenase reductase (Fe-protein) and

et al. (2001), extra-radical hyphae of AM fungi have the poten-

(2) dinitrogenase metal cofactor. The former enzyme serves as an

tial to protect the intracellular bacteria of the genus Burkholderia.

exclusive electron donor with high reducing power whereas the

One of the most important ecological signiﬁcance of these bacte-

later (substrate reduction component) accepts the electrons energy

rial genera associated with fungi is to have the potential ability

and convert inert N2 molecule into NH3. In order to produce one

to ﬁx atmospheric N , either in the nodules or as free living form.

mole of NH3, 16 moles of adenosine triphosphate (ATP) is required 2

In this association, bacteria reside in the thickest host structures

by these microbes (Hubbell and Kidder, 2009), who obtain this

(i.e. mycelium) to shelter the enzyme complex from oxygen and ﬁx

energy by oxidizing organic molecules. Free-living bacteria must

atmospheric N in this structure (Minerdi et al., 2001). However,

obtain this amount of ATP from other organisms, while photo- 2

the mechanism to ﬁx N in the mycelium (Kneip et al., 2007), still

synthetic microbes (cyanobacteria) use self-generated energy from 2

needs to be determined and need continuous research efforts to

photosynthesis process. Other microbes like associative and sym-

focus on this area especially for the recovery of nutrient depleted

biotic nitrogen-ﬁxer get these compounds from the rhizosphere

degraded soils.

of their host plant (Hubbell and Kidder, 2009). The chemical reac-

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

Table 1

Differences 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 metabolic Fungi do not ﬁx N but provide growth limiting nutrients (i.e.,

process. Bacteria from family Rhizobiaceae living in the soil carbon and P) to bacteria for N ﬁxation. Also, in mycelium,

infect plant root to form nodules and ﬁx N in this structure fungi provide shelter to bacterial enzyme system from O2 to ﬁx

through complex enzymes system. N.

2 Phosphorous (P) P solubilization or availability is enhanced by P mineralization Increase P bioavailability through mineralization in soil,

as well as well as production of siderophores and organic acids mycelial transport, P solubilization by siderophores, N

in the soil. assimilation and CO2 release.

3 Potassium (K) Bacteria release various types of organic acids to solubilize K in Inﬂuence K mobilization through mycelial transport as well as

the soil through various processes such as acidolysis, chelation, by K solubilization process that involves the release of H , CO2

complexolysis and exchange reactions. and organic acid such as citrate, malate and oxalate.

4 Iron (Fe) Production of siderophores which has afﬁnity to chelate and Translocate Fe from mineral to organic soil horizon for

solubilize iron from mineral or organic compounds. decomposition and mineralization, and release chelator

(siderophores) for Fe translocation in soil.

5 Aggregate formation Produce peripheral slime polymers and decompose organic Hyphal network entrap soil particle and forces them together.

material to form organo-mineral products that are associated Production of mucilages, polysaccharides and extracellular

with soil particles to form aggregates. compounds as well as soil proteins such as glomalin and

hydrophobins.

3.1.1. How do fungi inﬂuence N2 ﬁxation? suggested that global P production will reach to maximum by 2033

As discussed above, fungi indirectly affects N2 ﬁxation through (Cordell et al., 2009) while other researchers had concluded that

bacteria present in mycelia. During this process, fungi translocate almost 50% of the currently available P reserves will be mined by

carbon and P from the plant roots to the associated bacteria for N2 2100 (van Vuuren et al., 2010).

ﬁxation. In this regard Paul and Kucey (1981) observed a symbiotic In most of the agricultural soils (productive or degraded), huge

association of bacteria and fungi with legumes, which may indi- reserves of inorganic or organic P are present in immobilized or

cate a competition between these microbes for carbon provided by unavailable form. Fonte et al. (2014) observed no difference in

legume roots. However, this competition is masked by the associ- total P in degraded and productive pasture, however in this study,

ation of AM fungi with Rhizobia who provides a high amount of P organic P was 40% higher in latter pasture soil. They explained this

for nitrogenase enzyme complex (Puppi et al., 1994). The enhanced by showing the presence of higher inorganic P in degraded than

N2 ﬁxation ability of the bacteria through AM association is dete- productive pasture which was strongly adsorbed or occluded in

riorated by the depletion of P zone in mycorrhizosphere. AM fungi this soil. In fact, inorganic P is highly reactive with some metal com-

also provide plant derived carbon to increase the potential ability plexes such as iron, aluminum and calcium (Fig. 2), which lead to

of non-symbiotic N2 ﬁxer such as Herbaspirillum and Azospirillum. 75–90% of P adsorption or precipitation in the soil (Igual et al., 2001;

During this association, AM fungi decrease the total amount of sugar Gyaneshwar et al., 2002); Fig. 2). Even after the application of P fer-

and enhance nitrogenous compounds in mycorrhizosphere (Jones tilizers to the soils, a very low amount (micromolar) of P is available

and Oburger, 2011). The changes occurred in this region strengthen to plants as most of the P is adsorbed or becomes sparingly soluble

the carbon limitation of N2 ﬁxer over other microorganisms which (Gyaneshwar et al., 2002); Fig. 2). Microbial inocula such as bacteria

could limit their performance to ﬁx N2 (Veresoglou et al., 2012). (Han and Lee, 2005; Tao et al., 2008; Chang and Yang, 2009; Ma et al.,

On the other hand, non-symbiotic N2 ﬁxer are versatile organisms 2009; Yadav et al., 2014) mobilize native and inherited soil P as well

which possess the ability to adapt the carbon and N limiting condi- as any applied insoluble ﬁnely ground rock P. Such type of inocula

tions (Blaha and Schrank, 2003). Their performance is not affected are now termed as P-mobilizing microbes (Owen et al., 2015) rather

by the changes that occur in rhizosphere due to AM fungi colo- than previously referred as phosphate-solubilizing microorgan-

nization (Veresoglou et al., 2012). Therefore, it is not always true isms (Rodrııguez´ and Fraga, 1999; Rodriguez et al., 2004; Dastager

that AM fungi association with plant and rhizobia would be beneﬁ- et al., 2010; Jones and Oburger, 2011). As these inocula do not only

cial for long term recovery of degraded land as proposed by Chaer solubilize P, but they also mobilize its organic form through miner-

et al. (2011). In such condition, carbon limitation could be replen- alization (enzymatic hydrolysis) and facilitate the translocation of

ished by organic amendments in addition to the synergistic effect phosphate (Owen et al., 2015); Fig. 2). Microbes are responsible for

of co-inoculants such as N-ﬁxing bacteria and AM fungi. Such phe- mobilizing the soil P unavailable for plants through their direct and

nomenon needs to be further investigated for sustainable recovery indirect effects. In direct processes, (i) microbes solubilize P by low-

of degraded soils. In this regard, efforts are done to ﬁgure out the ering the pH (through proton extrusion) of external medium and

sole inoculation of N-ﬁxing bacteria or AM fungi with organic fer- producing low molecular weight organic anions (Fig. 2) like suc-

tilizers and obtained encouraging results for the rehabilitation of cinic, citric, gluconic, ␣-ketogluconic and oxalic acids (Chen et al.,

degraded land under semi-arid environment (Medina et al., 2010; 2006). These anions are exchanged for P on adsorption sites of soil,

Mengual et al., 2014a; Mengual et al., 2014b). the process commonly referred to as ligand exchange (Jones and

Oburger, 2011; Zhang et al., 2014). Hydroxyl and carboxyl groups

3.2. Phosphorus mobilization of these acids chelate the cations bound to phosphate thereby con-

verting it to soluble forms (Miller et al., 2010). (ii) In addition,

Phosphorus (P) is another essential and growth-limiting nutri- the inocula hydrolyze organic P compounds by producing phos-

ent in agro-ecosystems (Smil, 2000). However, this limitation could phatases or phytases (Fig. 2). Besides there are several ways through

be fulﬁlled by external inputs to the soil in the form of organic which indirect mobilization of P can be carried out by these inoc-

as well as synthetic fertilizers (Fig. 2). The later form of fertilizer ula: (i) Microbes release CO2 during respiration which is dissolved

is formulated from the rock phosphate reserves. Therefore, many in water (present in the soil pores) to form carbonic acid, thus sol-

researchers are concerned about rapid diminution of the world’s ubilizing P by decreasing the pH of mycorrhizosphere (Marshner,

+ +

P reserves due to continuous mining for P (Cordell et al., 2009; 1995) (ii) Microbes release proton (H ) during assimilation of NH4

van Vuuren et al., 2010). Recently, there is a contradiction in views as a result of which the soil pH is lowered and hence solubilize the

regarding the availability of world P reserves. Simulation studies available P (Illmer and Schinner, 1992) (iii) P solubilizing microbes

M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41 31

Fig. 2. An overview of the mechanism used by bacteria and fungi to mobilize nutrients (P, K and Fe) in the soil. Indicates processes carried out by microbial inocula

to enhance nutrient bioavailability. Speciﬁes primary intermediary steps. Speciﬁes secondary intermediary steps. Microbial inoculum.

have the ability to remove and assimilate phosphate from the soil Rhizoglomus intraradices) (Sieverding et al., 2014). In degraded soil

in order to re-establish the P equilibrium, in this way they stimulate (acidic), K solubilization was higher than calcium and magnesium

the indirect dissolution of Ca–P (Halvorson et al., 1990); (Fig. 2). after inoculation of AM fungi compared to un-inoculated control

(Clark et al., 1999). Inoculation of Aspergillus terreus and Aspergillus

3.3. Potassium niger increased the K level in soil solution by solubilizing K from

insoluble feldspar and potassium aluminum silicate (Prajapati et al.,

Potassium (K) is another vital nutrient and considered as a key 2012). This was related to the production of organic acids espe-

parameter of soil fertility and plant growth. In most of the soils, K cially by A. terreus which shows higher K solubilization than A.

is present in very small amount ranging from 0.04 to 3%. Despite niger . Moreover, other studies have reported that A. niger also pro-

being in limited amount, 98% of this K is bound within phyllosili- duce organic acids and trace elements during rock solubilization

cates structure (Shelobolina et al., 2014). This is the layer of silicate (Vandenberghe et al., 1999; Mirminachi et al., 2002).

minerals found in silt and clay fractions of the soil. The remaining

2% exists in soil solution or on exchange sites to become avail- 3.3.2. How do bacterial and fungal inocula increase K

able for the plants (Sparks and Huang, 1985). Hence, soil fertility is mobilization?

decreased due to low availability of this nutrient which is normally The major processes involved in mobilizing K are acidolysis and

fulﬁlled by commercial fertilizer (i.e., KCl), thus elevating the input complexolysis exchange reactions (Uroz et al., 2009). During aci-

cost of the farmers. Recently, few microbial strains were isolated dolysis, soil inocula such as bacteria or fungi decrease the local pH

who had an ability to oxidize in the ﬁrst step Fe from primary by producing succinic, citric, gluconic, ␣-ketogluconic and oxalic

phyllosilicates mineral in such a way that they release iron and acids (Fig. 2). Production of protons (H ) and organic acids anions

K from these minerals (Shelobolina et al., 2014). Bacterial inoc- not only enhances the chelation of cations which are bound to K but

ula (Neutrophillic lithotrophs) utilize structural Fe in biotite as an also helps for acidolysis of surrounding environment of microbes

electron donor for their metabolism in order to produce energy (Uroz et al., 2009; Zarjani et al., 2013; Parmar and Sindhu, 2013).

and oxidize biotite (Shelobolina et al., 2014). The microbes which During the process of acidolysis, rhizospheric microbes can chelate

oxidized biotite (Fe -bearing mica) include Bradyrhizobium japon- Al and Si cations associated with K minerals and by doing so they

icum, Cupriavidus necator, Ralstonia solanacearum, Dechloromonas also enhance the exchangeable K in soil solution (Römheld and

agitate, and Nocardioides sp . In addition to this, Sheng and He Kirkby, 2010). Consequently, microbes not only synthesize but also

(2006) suggested that inoculation of B. edaphicus NBT strains and discharge H , inorganic and organic acids to acidify their own cells,

its mutants increase the production of citric, oxalic, tartaric, suc- rhizosphere and surroundings of K minerals. This play an impor-

cinic, and ␣-ketogluconic acid. These acids lead to K mobilization tant role in mobilizing or solubilizing insoluble form and structural

from K-containing minerals (e.g. mica, biotite, kaolinite and smec- unavailable forms of K compounds in to soil solution resulting an

tite) and chelation of silicon ions (Han and Lee, 2005; Sheng and increased K availability in rhizosphere (Goldstein, 1994; Abou-el-

He, 2006). Seoud and Abdel-Megeed, 2012).

3.3.1. Fungi and K mobilization 3.4. Role of bacteria in Fe mobilization

In addition to bacterial strains, mineral form of K is solubilized by

fungi through releasing organic acid anions which mainly includes Iron is the fourth most abundant element available on earth

citrate, malate and oxalate (Meena et al., 2014). According to Wu and predominantly exists in nature in ferric (Fe ) form. It is

et al. (2005), K uptake was increased in corn crop after inoculation considered as one of the key micronutrient for soil fertility and

of G. mosseae (now, Funneliformis mosseae) and G. intraradices (now, is also needed by all kind of living organisms. It is sparingly

32 M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41 (2005)

(2004) (2004)

) al.,

(2010) et

(1999)

(2001 )

Höﬂich, Höﬂich,

(2015)

2009)

) (2004) 2010 and and

(2015) Fraga, al.,

Milic,

(2006) (2007)

(2003)

(2005) (2005) 2005; (2005) (2000) al., (2013) et

al.,

(2014)

(2014) al.,

(2002)

De–Bashan,

(2001)

and (2015) al.,

and (Yang, He,

al.,

(2005) (2008) (2005) al., et al., (2015) (2015)

(2009)

al., al.,

Lee, Lee, Lee, Lee, et al.,

al.,

et al.,

and

et and al., al., al., et al., al.,

et al.,

´ et ıguez

and and and and et et et

et et et

Dastager Reference Song Goswami Prakamhang Yadav Tytova Han Han Sheng Sharma Vansuyt Riggs Mrkovacki Wu Egamberdiyeva Egamberdiyeva Bashan Malik Tao Chang Ma ( Rodriguez Wu Zhang Cui Cui Han Han Rodrı Biswas acids

–ketogluconic ␣

and

succinic,

tartaric, acid

acids

acid acid

oxalic,

amino

– – – – OA Hydrocyanic – Free – – Citric, – – – – – – – – – – – – – Gluconic – – – – Gluconic –

– – – – √ √ √ √ OM – – – – – – – – – – – – – – – – – – – – – –

√ √ Fe – – – – – – – – – – – – – – – – – – – – – – – √ –

– – – – K – – – – – – – – – – – – – – – – – – – – – – – √

√ √ – √ – – – – – – – – √ – – – – √ √ √ √ √ √ √ √ P √ – –

– – – √ √√√√ √ √√√√ √ √ √ √ √ √ √ – √ √ √ √ √ – N – – – – – – – – –N/A

cepacia

acids.

parameters. Burkholderia brasilense organic

and

THA6

fertility

soil cepacia,

Azospirillum

matter,

B.japonicum

organic

improving

and

in chroococcum Pseudomonas

brasilense

B–6018

agglomerans USDA110

UCM involved

herbicola,

zotobacter spp –

C7 potassium, BS8 A

PsA15 =

Azospirillum

Pantoea K

MbP18 strains

GRP3

Erwinia

japonicum

diazoefﬁciens phlei

spp.

aeruginosa aeruginosa strain ﬂuorescens alcaligens alcaligenes spp., spp.

spp. lipoferum, spp. Burkholderia spp.

spp chroococcum

bacterial

leguminosarum

inoculant.

pneumonia,

spp, megaterium mucilaginous of

phosphorous,

various

megaterium mucilaginosus edaphicus megaterium natatu guianensis

effect of

Bacteria Rhizobacteria Pseudomonas Bradyrhizobium Pseudomonas Bradyrhizobium B. B. B. Pseudomonas Pseudomonas Klebsiella Azotobacter Azotobacter Pseudomonas Mycobacterium Azospirillum Azospirillum Bacillus Streptomyces Achromobacter Microccocus Azospirillum Bacillus Pseudomonas P. S. Bacillus B. Pseudomonas Rhizobium 2

Nitrogen, 1 2 3 4 5 7 8 9

Positive 10 20 No. 11 12 13 15 16 17 19 22 24 26 27 28 29 31 32 18 14 25 23 21 =

Table N Examples √

M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41 33

Table 3

Examples 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 = Nitrogen, P = phosphorous, K = potassium, OM = organic matter, AF = aggregate formation, GP = glomalin protein, AS = aggregate stability.

√–N/A

Positive effect of inoculant .

soluble, therefore not readily available for plant or other biota like through inﬂuencing energy production pathways (Minerdi et al.,

microbes in aerated soil. Moreover, in soil, ferrous (Fe ) is oxi- 2001; Mortimer et al., 2008). Bacteria enhance P availability for

dized to Fe thereby forming insoluble compounds and leaving a uptake of AM fungi and plant through phosphatase enzyme and

very low amount of iron for microbial or plant assimilation (Ma, organic acid production in the soil (Owen et al., 2015). Thus, their

2005). Therefore, to fulﬁll iron requirement for normal growth, co-inoculation tends to increase P and N availability in soil (Table 4).

tough competition exists among bacteria, fungi and plant in the rhi- Both fungi and bacterial inocula increase the nutrient availabil-

zosphere. In such circumstances, some strains of bacteria (Sharma ity in the soil solution through organic matter decomposition, N

et al., 2003; Vansuyt et al., 2007) synthesize low-molecular mass ﬁxation, P, K and Fe mobilization (Fig. 2). For instant, effect of

proteins known as siderophores. These molecules have high afﬁn- co-inoculation of plant growth promoting bacteria and Bradyrhi-

ity to chelate (Machuca et al., 2007; Miethke and Marahiel, 2007) zobium increase the soybean seed yield up to 44% per hectare than

and solubilize iron from mineral or organic compounds. Generally, their lone (single) inoculant form (Prakamhang et al., 2015). Sim-

siderophores have high afﬁnity to form complexes with Fe (1:1). ilarly co-inoculation of B. thuringiensis or Ps. putida with AM fungi

Uptake of the complexes by the cell membrane of both Gram posi- increase P by 44 and 35% in Trifolium repens respectively, while K

3+ 2+

tive and negative bacteria reduces Fe –Fe . Later cell membrane content was increased by 128 and 285%, than their lone inocula-

expel these ions from the siderophores into the cell (Boukhalfa and tion (Oritz et al., 2015; Table 4). Hence, interactions among soil

Crumbliss, 2002) by linking its inner and outer membranes, a mech- microbes in the soil rhizosphere positively affect soil fertility and

anism called “gating”. In this way siderophores solubilize iron from provide highly valuable ecosystem services. Therefore use of these

unavailable minerals or organic compounds in iron limited con- inocula can be exploited in order to increase yield, reduce chemical

dition (Indiragandhi et al., 2008). Additionally, bacteria produce inputs, and develop an efﬁcient form of sustainable fertilizer man-

extracellular siderophores which deprive pathogenic organisms agement in agro-ecosystems (Bhattacharjee et al., 2008; Nguyen

produced under Fe limited condition and form complexes with and Bruns, 2015; Owen et al., 2015) especially in degraded soils.

other heavy metals (Zn, Pb, In, Cu, Ga, Cd and Al) (Schalk et al., In general, it is very clear from the above mechanistic discus-

2011) and radionuclides including U and Np (Kiss and Farkas, 1998; sion that lone microbial inoculum could not be very effective in

Neubauer et al., 2000). Presence of such heavy metals encourages inﬂuencing the bioavailability of various nutrients (Table 4); there-

the bacteria to produce siderophores which chelate the metal to fore co-inoculation of microbes could prove to be more beneﬁcial

increase Fe availability in the rhizosphere of these soils (Wang et al., in recovery of degraded soil. However, some strains of bacteria

2002). Such bacteria play a vital role in elevating heavy metal con- or fungi can possess more than one mechanism and may prove

centration by phytoextraction through enhancing the activity of to withstand under water limited or nutrient depleted condition,

antioxidants. Hence, siderophores produced by microbial inocula therefore could be potential option for reinstating the lost functions

also play a key role in alleviating the stresses imposed on plants of degraded soils.

through heavy metals.

4. Soil structure

3.5. Interaction between bacteria and fungi inocula to improve

nutrient bioavailability in soil Destruction of soil structure is one of the most important indi-

cator of soil degradation which is mainly caused by loss of organic

Fungi and bacterial inocula interact with plant roots to improve matter through intensive soil management practices and land use

nutrient availability in soil for plant uptake (Glick, 1995; Smith and changes (Oldeman et al., 1990; Montgomery, 2007). However, soil

Read, 2010; Prakamhang et al., 2015); Tables 2 and 3). For this pur- structure plays a central role in crops management and thus agri-

pose, the co-inoculation between bacteria–bacteria, fungi–fungi or cultural ecosystems sustainability (Rillig et al., 2002). This can

bacteria–fungi species is also signiﬁcantly acknowledged in recent be deﬁned as size, shape and three dimensional arrangements

studies (Tytova et al., 2013; Leifheit et al., 2015; Nguyen and Bruns, of organic or mineral complexes (aggregates) and pores in such

2015; Ortiz et al., 2015; Prakamhang et al., 2015). In these inter- a manner that affect pore continuation, water inﬁltration and

actions, mycelium of AM fungi release carbon compounds which water holding capacity (Bronick and Lal, 2005). According to Tisdall

will act as energy source for soil microorganisms in the mycor- (1994), soil structure is an arrangement of individual soil parti-

rhizosphere, though the carbon products are in small amount than cles formed from sand, silt and clay. These are bound together

already present in rhizosphere (Andrade et al., 1997). Similarly, bac- through organic, inorganic or chemical forces in order to form

teria also exude carbon compounds which increase the AM fungi aggregates. Single particles adhere together more strongly with

hyphal growth and its root colonization (Barea et al., 2005). Dur- surrounding particles to form micro-, (<250 ␮m) and macroag-

ing the interaction among Rhizobia, AM fungi and legume, AM gregates (>250 ␮m diameter) size fraction (Kemper and Rosenau,

fungi enhance the growth and yield of legume by providing water 1986). Soil aggregates support root growth, a wide array of soil

and nutrients, especially P which increases Rhizobium N2 ﬁxation functions and ecosystem processes. These include carbon storage

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

Table 4

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

fertility and structural parameters.

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

Single inoculant √ √ √ √ √

√

1 i. Bacillus megaterium, Ortiz et al., 2015)

ii. Bacillus thuringiensis

iii. Ps Putida

√ √ √

2 i. Bacillus megaterium – – – (Armada et al., 2014)

ii. AM fungi √

√ √ √√

3 i. Bacillus megaterium, – (Mengual et al., 2014a)

ii. Bacillus thuringiensis

iii. Enterobacter s √

√

4 i. Rhizophagus irregularis – – – – (Leifheit et al., 2015)

ii. Natural soil microbes √

√

5 i. Piriformospora indica – – – (Kumar et al., 2012)

ii Pseudomonas R81

Co-inoculant

1 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 fertilizer

−

1 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 = Nitrogen, P = phosphorous, K = potassium, OM = organic matter, AF = aggregate formation, GP = glomalin protein, AS = aggregate stability. –N/A

Positive effect of inoculant .

and resistance to erosion (Jastrow et al., 1998; Six et al., 2004). form slightly larger aggregates (20–250 ␮m diameter) (Miller and

Soil structure is mainly articulated by the degree of aggregate Jastrow, 2000). Moreover, during bacterial growth, extracellular

stability (Amezketa, 1999). Organic matter is one of the main polymeric substances are produced in the form of peripheral slime

agents in aggregate formation and stabilization. Therefore, increas- polymers into soil solution (Aspiras et al., 1971); Fig. 3). These are

ing organic matter in soil is very vital for the rehabilitation of negatively charged polysaccharides, polyuronic and amino acids

degraded soils. Other factors involved in this process are persistent with adhesive properties capable of making bond between clay par-

cementing agents like humic acid that stabilizes microaggregates ticles in order to form aggregates (Tang et al., 2011; Caesar-Tonthat

and polysaccharides derived from plants as well as microbes. Fun- et al., 2014). These aggregates adhere together to form macroaggre-

gal hyphae, plant roots and bacteria are temporary binding agents gates (>250 ␮m diameter) and thus increase inter-particle cohesion

in the formation and stabilization of macroaggregates (Tang et al., (Degens, 1997).

2011). A critical aspect in this regard is the formation of water stable

aggregates which are part of the macroaggregates (>250 ␮m). They

are known to remain stable and fail to dissociate with frequent soil

4.2. Fungi and soil aggregation

wetting and drying cycles (Sun et al., 2014). Soil aggregation sta-

bility is a multifaceted process and is an indicator of many aspects

The omnipresent AM fungi use its extra-radical hyphae

of soil structure including erosion, soil water regime and nutrient

(mycelium) to stabilize soil aggregates (Rillig et al., 2006; Bedini

availability. The stability of aggregates is controlled by soil phys-

et al., 2009; Peng et al., 2013) as well as it can modify the mor-

ical, chemical, and/or microbial community properties and plant

phological structures and biochemical nature of host plants (Borie

roots (Zadorova et al., 2011; Graf and Frei, 2013; Pérès et al., 2013).

et al., 2008) including its roots and rhizosphere. Additionally, AM

Among soil microbes, AM Fungi symbionts typically represent a

Fungi can also alter soil microbes in its surrounding environment as

major force in stabilizing macroaggregates than bacteria (Tang

well as the rhizosphere of host plant which are probably involved

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

in soil aggregation (Mansfeld-Giese et al., 2002; Rillig et al., 2006;

Caesar-TonThat et al., 2007). These contributions of AM fungi are

often entangled together (Kohler-Milleret et al., 2013). According to

4.1. Bacteria and soil aggregation

Bedini et al. (2013), mean weight diameter of aggregate (an indica-

tor of stability) is strongly correlated with hyphal length of fungi but

Inﬂuence of bacteria on soil aggregation is dependent on soil tex-

weakly with root volumes. On the other hand Glomus geosporum, F.

ture and nutrient availability (Degens, 1997). They reside mainly in

mosseae, or G. intraradices (now R. intraradices) do not affect aggre-

the form of individual cells, microcolonies or bioﬁlms in the aque-

gate size distribution and stability in sandy loam soil (Martin et al.,

ous solution within the pores of soil aggregates, thus ensuring that

2012). Daynes et al. (2013) developed a model for soil aggregation

they may attach to surfaces of microaggregates (Fig. 3). Bacteria

where their simulated results indicate that AM fungi, organic mat-

decompose organic material to form organo-mineral products that

ter and plant roots are key contributors to aggregate formation in

are associated with soil particles to form stable microaagregates

soil. They also observed that this group of fungi plays an important

(2–20 ␮m diameter) (Tisdall, 1994). These small microaggregates

role in stabilization of soil aggregates.

are in turn bound by bacterial and saprophytic fungi products to

M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41 35

Fig. 3. An overview on the role of bacterial and fungal inocula in the formation of soil aggregates.

4.2.1. How do fungi inﬂuence soil aggregation? Mechanism 4.3. Interaction between fungi and bacteria to improve soil

Mycelium of AM fungi impacts soil aggregation through com- aggregation and their stability

plicated direct and indirect mechanisms which are strongly

interdependent (Fig. 3). In direct mechanism, hyphal network of Fungi inﬂuence microbial communities in the soil rhizosphere

AM, ectomycorrhizal, saprophytic and others fungi entraps soil through many ways (as discussed above) and the interaction facili-

particles and forces them together (Tisdall, 1994; Peng et al., tated by AM fungi leads to changes in the turnover and distribution

2013; Zheng et al., 2014). On the other hand, Chenu et al., 2002 of soil aggregates. However, these changes are arbitrated, and the

reported that hyphal network aligns soil particles along its expand- prominence of these changes to soil aggregation and other medi-

ing hyphae to form aggregates (Fig. 3). During indirect mechanism, ated processes are poorly deﬁned (Rillig et al., 2006). Fungi deposit

mycelium exudes glomalin, hydrophobins and related soil proteins organic compounds in the mycosphere through mycelium which

as well as mucilages, polysaccharides and extracellular compound act as a substrate for the growth of microbes (bacteria and fungi).

into the soil (Rillig et al., 2006; Caesar-TonThat et al., 2013). Accord- Bacteria isolated from fungal mycelium prove to be very impor-

ing to Driver et al. (2005), about 80% of glomalin protein is bound tant in formation of soil aggregates. According to Caesar-TonThat

in hyphal wall which helps in transporting nutrients and water for et al. (2013) Pseudomonas ﬂuorescens and Stenotrophomonas mal-

AM fungi. It protects the fungal hyphae and lipid rich spores from tophilia isolated from Agaricus lilaceps fruiting body binds soil more

drought and microbial attack which form clumps of soil aggre- than Bacillus sp. isolated from outside and inside of the fairy ring.

gate through decomposed hyphae, glomalin protein fused with Additionally, fungal activity can alter nature and extent of availabil-

minerals (sand, silt and clay) and organic matter (Borie et al., ity of pore spaces in the soil for the habitat of other surrounding

2008). Glomalin is hydrophobic protein which contributes to the microbes. This is in accordance with Gupta and Germida (2015)

hydrophobicity of soil aggregates. In addition to this, the glue-like who reported that distribution of microbial diversity in soil is con-

nature of glomalin also helps in the initiation and stabilization of trolled by pore structure and aggregate hierarchy. Consequently,

aggregates (Miller and Jastrow, 2000) and may act as adhesive microbial biomass, bacteria and fungi community composition, as

agent to bind soil particles together (Chenu, 1989; Wright and well as their functional attributes vary within aggregate sizes (Chen

Upadhyaya, 1996). Saprotrophic fungi produce extracellular exu- et al., 2015; Gupta and Germida, 2015).

dates that promote water stable aggregates (Ambriz et al., 2010). In addition to rhizospheres microbes, AM fungi can potentially

Similarly extracellular mucilages like polysaccharides exuded by inﬂuence soil aggregation by affecting plant communities, plant

basidiomycetes and Trichocomaceae bind the soil particles into roots (individual host), and soil fauna such as earthworms, termites

aggregates and increased their stability (Caesar-TonThat, 2002; or ants. These biota are considered to be key soil engineers (details

Daynes et al., 2012). Some species of ectomycorrhizal fungi exudes about these biotic interaction are not within the scope of this arti-

hydrophobic compounds which are important in exploring large cle) for pore size distribution and soil aggregation (Rillig et al., 2015;

distance in the soil for transporting nutrients and water for fungi Bottinelli et al., 2015; Maaß et al., 2015). Fungal hyphae and plant

(Agerer, 2001) Fig. 3). Hydrophobins are small proteins, considered roots binds and stabilize macroaggregates (>250 ␮m) in particular

to affect soil wettability and water repellency from the aggregates (Tisdall and Oades, 1982) whereas microaggregates (<250 ␮m) are

(Diehl, 2013). By exuding hydrophobic compounds, fungi tend to stabilized by eternal binding agents like bacterial polysaccharides

increase hydrophobic soil organic matter that can avoid breakage (Daynes et al., 2012); Table 3). Thus it is very likely that soil aggre-

of dry soil aggregates in the rewetting process and thus creat- gation is the results of numerous interconnecting components or

ing more water stable aggregates (Six et al., 2004). This could be processes which are driven by different set of traits epitomized in

in line with more recent ﬁndings of Xu et al. (2015) who had different species (Rillig et al., 2015). Therefore, to reinstate the soil

reported that AM fungi increased soil organic carbon which was structure in degraded soils, it would be unwise to rely only on one

positively related to normalize mean weight diameter of aggre- or two components. Instead, the process is cumulative involving

gates. They suggested that increase in soil organic carbon by AM various factors such as plant root, soil biota (microbes and animal)

fungi could be a mechanism through which fungi improve soil and organic matter that could be enhanced by activities of soil life

structure. as well as addition of organic fertilizers.

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

5. Organic amendments to reinstate soil fertility trin, 2,4-diacetylphloroglucinol, pyoluteorin, viscosinamide and

tensin). Hence they act as biocontrol agent in various diseases and

Organic amendments such as animal manure (solid cattle environmental stresses (Bhattacharyya and Jha, 2012; Goswami

manure and slurry), compost and crop residues could play an et al., 2015). Ectomycorrhizal and AM fungi also increase the soil

important role in enhancing the fertility of degraded soil. These nutrient and water transport through soil exploration by their

amendments increase the organic matter and thus inﬂuence the hyphal network/pipelines and production of organic acids to mobi-

soil life by providing them a source of food. Enhancing soil lize the ﬁxed nutrients (Andrade et al., 1997; Barea et al., 2005;

organic matter is the most important step to rehabilitate the Mortimer et al., 2008; Caesar-TonThat et al., 2013). AM Fungi can

strongly degraded land. Since this parameter play a signiﬁcance mobilize N, P, K, Fe and other nutrients in the soil and transfer these

role in increasing the capability of the ecosystem to support the nutrients to the host plants (Smith and Read, 2010) through translo-

more diverse and complex community composition, formation of cation process by hyphal network (Fig. 2). AM fungi can reduce N

soil aggregates, maintenance of soil structure, fertility and water and P losses (Asghari and Cavagnaro, 2012) through leaching and

holding capacity (Tiessen et al., 1994; Kononova, 2013). Rashid N2O emission (Bender et al., 2015) and enhanced nutrient intercep-

et al. (2014a) observed that continuous application of solid cat- tion of AM fungi rooting systems. Due to these activities, microbial

tle manure increased organic matter, N, pH, microbial biomass and inocula drive nutrient cycling and at the same time also deter-

soil fauna in sandy soil compared to that of slurry manure fertiliza- mined whether these nutrients are made available to plants. By

tion. Application of urban refuse increased soil microbial activities doing so, these microbial inocula can achieve satisfactory results in

as well as AM fungal diversity in degraded soil of semi-arid region the restoration of degraded soil. Seneviratne et al. (2011) observed

(del Mar Alguacil et al., 2009). In addition to these studies, use of that application of bioﬁlm based fertilizers developed from N2 ﬁxer

poultry manure and wheat straw in degraded soil of Himalayan bacteria increased N2 ﬁxation and soil organic carbon. Hence, these

region increased organic matter content, hydraulic conductivity, fertilizers stimulated the ecosystem functioning and help in achiev-

aggregate stability, N, P, K, carbon sequestration and pH compared ing sustainable restoration of degraded agricultural soil within few

to urea or unfertilized control (Khaliq and Abbasi, 2015). Combine months in tropics. Microbial communities present in these bioﬁlm

application of solid cattle manure and chemical fertilizer increased based fertilizers substantially enhanced the microbial biodiversity

soil organic matter, N, microbial biomass and the crop productivity which leads to sustainability of agro-ecosystem and environment

and reduce the decreasing stock of soil carbon (Srinivasarao et al., (Seneviratne et al., 2011).

2014). Tian et al. (2015) found that application of bio-solids with

high stable carbon and low carbon:N increase carbon sequestra-

tion rate of crop residues than un-amended soil. They concluded

that use of such organic amendments in agricultural soil is a valid

approach to transform them from current carbon-neutral status to a 5.2. Application of bacterial and fungal inocula with organic

carbon sink. Moreover, application of bio-solids and vegetative yard amendments to reinstate the fertility of degraded land

compost increased fungal biomass and enzymatic activity in indus-

trial degraded soil compared to un-amended control during the ﬁrst Few researchers use combination of bacteria or fungi inocula

year of application however enzymatic activity was declined in the with organic amendments to reinstate one or few parameters of

second year (Carlson et al., 2015). Therefore, such ﬁndings could degraded soil in controlled experiments and obtained promising

restrict the lone use of organic amendments for the nutrient man- results (Medina et al., 2004; Mengual et al., 2014a,b; Leifheit et al.,

agement of degraded soil and may urge researcher to think of more 2015). For instance, Leifheit et al. (2015) used fungal inoculum with

mixed management option rather than simple solutions. organic residues to increase soil aggregation and their stability in

pot experiment while Mengual et al., (2014a,b) found increase in

5.1. Bacterial and fungal inocula to reinstate the fertility of soil P availability, total N and other microbiological and biochemical

degraded land parameters with co-application of bacterial inocula and composted

sugar beet in small ﬁeld assay. Recently it was found that combined

Bacterial and fungal inocula play an important role in the effect of bacterial and fungal inocula and cover crops increased P

restoration of degraded soil. Singh, (2014) reported that cyanobac- mobilization and soil organic matter in subtropical red soils dur-

teria ﬁx atmosphere N2 in degraded soils and release extracellular ing a time duration of six months (Cui et al., 2015). They found

polysaccharides, which are metabolized by the associated soil that P. natatu tends to increase the soil organic matter by 5.2%

−1

microorganisms. In addition, other bioactive compounds produced (17.97 ± 1.02 vs. 17.07 ± 1.05 g kg ) from control but it was not sta-

by these bacteria positively inﬂuence soil fertility, decrease soil tistically signiﬁcant while inoculation of AM fungi further enhanced

pathogens and therefore improve crop growth (Singh, 2014). Bio- this parameter by 5.4% (18.94 ± 1.03 vs. 17.97 ± 1.02, P > 0.05) from

logical N2 ﬁxing bacteria encourage the growth and persistence P. natatu. Moreover, in this study moderately labile organic P was

of other soil microbial groups in the rhizosphere by providing also increased from control (302.8 ± 4 vs. 272.5 ± 9.2, P = 0.05). This

N (Seneviratne et al., 2008). Similarly bacteria exude extracel- form of P strongly inﬂuence the phosphomonoesterase enzyme

lular polysaccharides that promote soil aggregations (Degens, activity (Cui et al., 2015). Hydrolytic enzymes released by soil inoc-

1997). Bacterial strains also mobilize the ﬁxed or unavailable ulants are main drivers of carbon, N and P cycling hence they

P, K and Fe in the soil (discussed in various sections). In addi- play a key role in hastening the nutrients cycling in soils for plant

tion to this, bacterial inocula also produce phyto-hormones growth (Burns et al., 2013). Thus, a combined application of organic

(Auxin/Indole Acetic Acid) which improve plant defense against amendments, cover crops, fungal and bacterial inocula could be

various pathogens (Lugtenberg and Kamilova, 2009; Ahemad a good approach for the sustainable restoration of degraded soil

and Kibret, 2014; Goswami et al., 2015). These inocula also which is not considered yet under ﬁeld conditions. In above discus-

produce aminocyclopropane-1-carboxylate deaminase that pro- sion, it had been highlighted that direct application and symbiotic

motes the root elongation, shoot growth, and enhances rhizobial interactions of bacterial and fungal inocula with crops and organic

nodulation as well as N, P and K uptake in various crops fertilizers could be used as an emerging tool for restoring degraded

(Nadeem et al., 2009; Glick, 2012, 2015; Goswami et al., 2015). lands. Therefore, adequate selection for the combined application

Plant growth promoting bacteria induce systemic resistance of diverse communities of bacteria, fungi and organic fertilizers

and produce antifungal metabolites (HCN, phenazines, pyrrolni- could be a key to restore and reinstate the degraded ecosystems.

M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41 37

5.3. Gaps in current approaches and way forward to restore the 3. To achieve sustainability in crop production, studies regarding

degraded land microbial inocula should focus more on nutrient cycling (ﬁx-

ation, mobilization, translocation, leaching losses and gaseous

It is apparent from the above discussion that microbial inoc- emissions) rather than only single fate of the nutrient. There-

ula are one of the valuable bio-resources that could be helpful in fore the focus of future studies must be based on the processes

restoring degraded lands. However, most of the researchers use to understand the inﬂuence of microbial inocula on nutrient

lone bacterium or fungal strain in their experiments that can par- cycling.

tially result in the reported discrepancies at ﬁeld scale (Table 4). The 4. Bacterial and fungal inocula could be successfully employed in

reasons for lower response than co-inoculation could be that single reinstating fertility of degraded soils. However, their applica-

microbial inoculum is not likely to be active as it faces competition tions would consider the inherent limitations of these inocula

of resources from indigenous microorganisms in order to survive in and ﬁgure out the best strains of both bacteria and AM fungi who

soil environment (Singh, 2014, 2015). To make the inocula success- can establish a long-lasting association to improve the fertility

ful under ﬁeld condition, it could be fascinating to test whether the and structure of such soils.

combinations of ecologically diverse microbial strains, with akin

functions, and addition of organic fertilizers can meet the goal of

restoring the fertility of degraded lands. Such mixture of bacterial 7. Conclusions

or fungal inocula may create synergistic effects (Singh, 2015) while

organic manures can meet their nutrient demands to make them In the coming decades, land degradation will be major threat to

successful under ﬁeld conditions. These associative interactions the food security. Therefore most important issue is how to feed the

could be successful and may play a crucial role in restoring the pro- increasing population of the world where about 84% of agricultural

ductivity of degraded soils. However, ﬁeld experiments are lacking land per capita is declining and degrading due to its extensive use?

evidence to support these hypotheses. Singh (2015) proposed that Fungi and bacterial inocula and their combine use with organic fer-

successful restoration of degraded soil using microbes required a tilizers could be a promising approach for remediation of degraded

combined knowledge on microbiology, ecology, biochemical mech- soil and would help to limit the extensive use of chemical fertilizers.

anisms and ﬁeld engineering. Moreover, most of the soil functions Due to ﬁxation, chelation, production of organic acid, siderophores,

i.e. organic matter stabilization, decomposition, nutrient mobiliza- hydrophobins and glomalin protein, these microbes are capable of

tion, translocation and mineralization, and aggregate formation enhancing nutrient bioavailability and improving soil aggregation.

and stability are carried by microbes. To attain the sustainable pro- Hence they could be used in reinstating the fertility of degraded

ductivity in agro-ecosystems, the aforementioned soil functions soils. Understanding the mechanisms of microbial inocula in the

have not been fully explored due to complex microbial diversity provision or mobilization of nutrients in degraded land is a key

in these soil ecosystems. Therefore, it is very important to further for their success in ﬁeld applications. Although exact mechanisms

explore unidentiﬁed microorganisms that can live in competitive through which bacteria and fungi achieve these beneﬁts in such

environment under ﬁeld conditions and help to increase the soil soils are not fully understood, however it is becoming clearer that

fertility and productivity of degraded soils in order to meet the few or all traits of these microbes can allow them to perform their

increasing global food demand and at the same time environmental associated functions. To this end, a better understanding on the

sustainability. interaction of bacteria and fungi when applied under ﬁeld condi-

tions is required. The clariﬁcation of these mechanisms may help

in the development of innovative and cost effective management

6. Future considerations

practices for improving the fertility and crop production capac-

ity of degraded soils. Use of single inoculum or co-inoculation of

Bacteria and fungi are integral part of soil microbial commu-

bacteria-bacteria, bacteria-fungi or fungi–fungi could not always

nity. These microbes play a vital role in the restoration of degraded

be very fruitful for the reclamation of degraded soils. In fact, lone

soils through fertility enhancement by affecting nutrients cycles

or dual strains with distinct functions are less active and could

as well improvement in soil structure. Regardless of encouraging

not survive in nutrient deﬁcient soil environment due to compe-

evidences on the application of microbial inocula for improving

tition of resources for their survival. However, addition of organic

nutrient bio-availability and soil aggregation, still many aspects

fertilizer with co-inoculation of bacterial and fungal strains could

need to be explored for further studies which are as follows:

have a potential for restoration of degraded soils because organic

matter can fulﬁll the nutrient demand while bacteria and fungi

1. Many studies have revealed that the application of single bacte-

can create synergistic effect for nutrient acquisition as well as soil

rial or fungal inoculum or their co-inoculation to soil improves

aggregate formation and stabilization. Hence, inoculation of bacte-

its fertility and aggregation. In most cases, co-inoculation per-

ria and fungi with organic fertilizers can reduce the excessive use

formed better than their sole/lone counterpart (Table 4) but

of chemical fertilizers which are a serious concern for the farmers

there are still certain aspects that require serious attention such

(especially those producing crops on moderately degraded soils)

as evaluation of these approaches under ﬁeld conditions. Major-

as well as on the environment. Therefore the central decree of this

ity of experimental studies are carried out in laboratory or in

study is to realize that for complete restoration of degraded soils, a

the pots under controlled conditions, therefore performance or

combinatorial mixture of management practices is necessary. This

adaptability of these microorganisms under ﬁeld condition may

includes inoculation of soil biota (microbes and animal) in addition

differ signiﬁcantly. Under natural ﬁeld conditions, both biotic

to organic fertilizers, plant roots and other associated factor like

and abiotic factors are not controlled and the competition for

growing of cover crops.

resources is higher thus affecting their performance.

2. Application of organic fertilizers in combination with micro-

bial inocula could have a potential to reinstate the fertility Acknowledgments

and productivity of degraded land. However, adequate selec-

tion of microbial inocula to enhance their synergistic effect has

This review was supported by the Ministry of Higher Education,

not gained much attention from the scientiﬁc community. This

Kingdom of Saudi Arabia, Centre of Excellence in Environmental

needs to be further explored by the researchers.

Studies, King Abdulaziz University, Jeddah, Kingdom of Saudi Ara-

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

bia and Department of Environmental Sciences, COMSATS Institute Caesar-TonThat, T., Caesar, A., Gaskin, J., Sainju, U., Busscher, W., 2007. Taxonomic

diversity of predominant culturable bacteria associated with microaggregates

of Information Technology, Vehari, Pakistan.

from two different agroecosystems and their ability to aggregate soil in vitro.

Appl. Soil Ecol. 36 (1), 10–21.

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