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Bacteria and fungi can contribute to nutrients bioavailability and aggregate

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DOI: 10.1016/j.micres.2015.11.007

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 Microbiological Research 183 (2016) 26–41

Contents lists available at ScienceDirect

Microbiological Research
journal homepage: www.elsevier.com/locate/micres

Bacteria and fungi can contribute to nutrients bioavailability and

aggregate formation in degraded soils
Muhammad Imtiaz Rashid a,d,∗ , Liyakat Hamid Mujawar a , Tanvir Shahzad e ,
Talal Almeelbi a,b , Iqbal M.I. Ismail a,c , Mohammad Oves a
a
Center of Excellence in Environmental Studies, King Abdulaziz University, P.O Box 80216, Jeddah 21589, Saudi Arabia
b
Department of Environmental Sciences, King Abdulaziz University, Jeddah 2158, Saudi Arabia
c
Department of Chemistry, King Abdulaziz University, Jeddah 2158, Saudi Arabia
d
Department of Environmental Sciences, COMSATS Institute of Information Technology, 61100, Vehari, Pakistan
e
Department of Environmental Sciences & Engineering, Government College University, 38000, Faisalabad, Pakistan

a 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
Available online 25 November 2015
future generations. Implementing safe and environmental friendly technology would be viable solution
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:
Degraded land nutrient bioavailability through nitrogen fixation and mobilization of key nutrients (phosphorus, potas-
Food security sium and iron) to the crop plants while remediate soil structure by improving its aggregation and stability.
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.
© 2015 Elsevier GmbH. All rights reserved.

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: mimurad@kau.edu.sa (M.I. Rashid), irmaliks@gmail.com (M. Oves).

http://dx.doi.org/10.1016/j.micres.2015.11.007
0944-5013/© 2015 Elsevier GmbH. All rights reserved.
 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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
4.3. Interaction between fungi and bacteria to improve soil aggregation and their stability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
5. Organic amendments to reinstate soil fertility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
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. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .36
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
are omnipresent and found in various components of earth such as
water and soil.
Bacteria and fungi are also known to improve soil struc-
ture by promoting the formation of soil aggregates and pores
within (Degens, 1997; Miller and Jastrow, 2000). Fungal cells
release mucilaginous exudates which are mainly composed of
extracellular surface polysaccharides; cell wall polysaccharides
and somatic or intracellular polysaccharides located inside the
cytoplasmic membrane. Extracellular polysaccharides are mainly
responsible for the formation of aggregates, which are beneficial
for improving porosity and aeration in soil. Moreover, bacteria
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
influenced by the mineral constituents of the soil but also by the
presence of micro-organisms in pores (Gupta and Germida, 2015).
On the other hand, exudates from bacteria, fungi, decomposed cells
as well as plant and animal residues especially in soils managed by
organic inputs are also responsible to boost the soil organic matter
which in turn improve the soil structure, function and quality.
Reconnoitering the mechanisms of bacterial and fungal inoc-
ula together with organic fertilizer could be very valuable tool
for improving soil fertility (Song et al., 2015) and aggregation.
Such strategy may help in planning a chemical fertilizer-free, envi-
ronmental friendly integrated soil nutrient management to meet
global food demand which may further help in reinstating the
fertility of degraded soil. In this regard, various aspects of the
bacterial and fungal-mediated soil nutrient acquisition processes
and aggregate formation have also been recognized. Co-inoculation
of bacteria and fungi with organic amendments could be an elo-
quent approach for sustainable management of soil fertility and
crop production (Minerdi et al., 2001; Rillig et al., 2002; Mortimer
et al., 2008; Caesar-Tonthat et al., 2014) in strongly degraded soil.
In order to avail maximum benefits from such approaches, there
are still many undeveloped facets that need to be explored in
future studies. The mechanistic understanding of bacterial and
fungal-mediated soil nutrient enhancement and aggregation is still
underdeveloped. Novel field-based studies and experiments under
controlled conditions need to be planned to lend better accuracy in
the understanding of microbial influenced soil fertility and struc-
tural attributes. The main objective of present review is to highlight
and 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) and
aggregation. We will discuss the effectiveness of these microbes
when inoculated solely, as co-inoculant or in combination with
organic fertilizer in improving fertility and aggregation stability of
degraded soils.
2. Reinstating fertility of degraded soils
Land degradation is a worldwide problem caused by number
of human induced processes that result in loss of soil fertility and
productivity. The major causes of the land degradation includes
deforestation, improper agricultural practices, (intensive cultiva-
tion, unbalanced fertilization, poor quality irrigation and chemical
inputs in the form of fertilizers or pesticides) and industrializa-
tion (Dregne 2002). Moreover, Dlamini et al. (2014) have associated
land degradation with decrease in soil organic carbon and N stocks.
According to estimation by Bai et al. (2008), about 40% of the world
agricultural soils are seriously degraded whereas 24% area of the
productive soils is still under continuous degradation. This requires
special attention to figure out alternative and sustainable nutrient
management techniques that can reinstate the fertility of such soils.
Integrated management of microbial inocula and organic fertilizers
could be an alternative option which needs to be explored in future
studies. In the following sections, few approaches for restoring the
fertility of degraded soils are discussed. However, the limited focus
of following discussion will not provide complete guidelines for
attaining sustainable restoration of degraded soil, but it describes
few essential management options that could be important to con-
sider in this regard.
 M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41
2.1. Microbial inocula and soil nutrient bioavailability
Various species of bacteria and fungi play a key role in improv-
ing soil fertility. These microbes increase organic matter that boosts
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
and facilitate their plant uptake from the rhizosphere. The simi-
larities or differences in bacteria and fungi to influence nutrient
bioavailability and aggregate formation are discussed in Table 1.
In this manner, the application of chemical fertilizers in agro-
ecosystems can be greatly reduced (Figueiredo et al., 2011a). Hence,
application of microbial inocula would not only help the farmers to
reduce the additional costs of chemical fertilizers but also assist
in obtaining high crop yield. Most of the processes through which
microbial inocula promote soil fertility are not fully understood,
however it is believed that microbes use several direct and indirect
mechanisms (Glick, 2012). These are highlighted and reviewed in
forthcoming sections.
2.1.1. Nitrogen fixation
Nitrogen (N) is an essential nutrient required by plants for
their growth and metabolism. It is often lost through leaching or
emission thus limiting its availability in most of the cultivated
soils. Although N is present abundantly in atmosphere in the form
of diatomic (N2) molecule, but its structure makes N2 molecule
inert. However, reduction of N2 molecule into N is a complex pro-
cess which requires input of huge amount of energy (Postgate,
1982). Prokaryotic microorganisms known as diazotrophs fix atmo-
spheric N2 in the form of ammonia (NH3 ) through their normal
metabolic process (Riggs et al., 2001; Galloway et al., 2008). These
microbes are free living organisms present in the bulk soil (Reed
et al., 2011) that mainly includes Cyanobacteria, Proteobacteria,
Archaea, and Firmicutes (Demba Diallo et al., 2004; Duc et al., 2009).
Some of these organisms (Azotobacter and Azoarcus genera) are
also present at comparable densities in the rhizosphere and bulk
soil. However, there are other bacteria from genera Herbaspirillum
and Azospirillum that colonize only in the rhizosphere (Mrkovacki
and Milic, 2001; Malik et al., 2002; Bashan et al., 2004; Bashan
and De-Bashan, 2010). Rhizobia has the capability to infect roots
and induce the formation of root nodules (Stacey, 2007). There-
fore in the field of N fixation, most of the researchers specially
focus on rhizobium-legume symbiosis due to higher impact on
primary productivity of the agricultural ecosystem (Rengel, 2002).
The establishment of this association results in the formation of
highly specialized organ called ‘nodules’ that are formed on the
intracellular root of symbionts, on which bacteria colonize. Such
bacteria mainly belong to the family Rhizobiaceae that develop a
highly specific interaction with the infected root. This interaction
consists of several stages which involves the exchange of complex
signals between the bacterium and plant (Sprent et al., 1989). Bac-
teria fix N2 through a complex enzyme system called nitrogenase
(Kim and Rees, 1994) and this enzyme system exists as two sep-
arable components; (1) dinitrogenase reductase (Fe-protein) and
(2) dinitrogenase metal cofactor. The former enzyme serves as an
exclusive electron donor with high reducing power whereas the
later (substrate reduction component) accepts the electrons energy
and convert inert N2 molecule into NH3 . In order to produce one
mole of NH3 , 16 moles of adenosine triphosphate (ATP) is required
by these microbes (Hubbell and Kidder, 2009), who obtain this
energy by oxidizing organic molecules. Free-living bacteria must
obtain this amount of ATP from other organisms, while photo-
synthetic microbes (cyanobacteria) use self-generated energy from
photosynthesis process. Other microbes like associative and sym-
biotic nitrogen-fixer get these compounds from the rhizosphere
of their host plant (Hubbell and Kidder, 2009). The chemical reac-
29
tion of microbial N fixation (Postgate, 1998) is shown in following
equation.
N2 + 8 H+ + 8e− + 16MgATP → 2NH3 + H2 + 16MgADP + 16Pi
2.1.2. N2 fixation in degraded land
Phosphorus (P), potassium (K) and sulphur are generally lim-
ited in degraded soils. Under nutrient limited conditions, these
nutrients affect the N2 fixation by reducing the growth of N-fixing
bacteria, nodule formation and functioning, as well as affecting
host plant growth. Meta-analysis study of Divito and Sadras (2014)
confirmed that nodule production, activity and their number are
limited more than plant shoot biomass in response to the deficiency
of P, K and sulphur. Moreover, P limitation in soil decreases the
activity of nitrogenase enzyme in N-fixing bacteria, because both
autotrophic and heterotrophic bacteria require high ATP for cellu-
lar N2 fixation (Reed et al., 2007, 2011; Pérez et al., 2014). Similar to
nutrient deficiency, soil moisture is another major factor that influ-
ences nodule formation or retardation of nodule growth. Water
availability in soil is related to water holding capacity which is very
low in degraded soil (Montgomery, 2007). According to Sinclair
et al. (1987) water limiting conditions severely affect nodule for-
mation in soybean crop. Thus in degraded soils, N2 fixation and
other related functions (decomposition, mineralization, enzymes
or organic production) of microbes are severely affected due to loss
of fertility and water holding capacity. Soil microbes adapt vari-
ous strategies to cope with such deficiencies. These strategies are
discussed in the forthcoming sections.
3. Mechanisms used by microbes to reinstate the fertility of
degraded 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 the
bacteria to infect plant root. As indicated by Puppi et al. (1994) and
Nasto et al. (2014), AM colonization can fulfill high demands of P
required by nitrogenase enzymes for N2 fixation when inoculated
with N2 fixer rather than non-N2 fixer to increase the growth of
host plant. Many studies reported that co-inoculation of bacteria or
legumes with AM fungi increased N2 fixation ability of legumes or
trees (Ibijbijen et al., 1996; Bona et al., 2014). However, this increase
in N2 fixation ability does not necessarily mean that growth and
productivity of host plants will increase. Meta analyses studies by
Larimer et al. (2010) and Kaschuk et al. (2010) have shown that
co-inoculation of AM fungi with rhizobia or free living N-fixing
bacteria resulted in a non-additive effect on the growth of host
plant. However, plant growth responses were positive when AM
fungi or N2 fixer were inoculated alone. Extra-radical hyphae of AM
seem to have ability to fix atmospheric N2 through N-fixing bacteria
present in mycelia. According to Bianciotto et al. (1996) and Minerdi
et 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 ability
to 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 fix
atmospheric N2 in this structure (Minerdi et al., 2001). However,
the mechanism to fix N2 in the mycelium (Kneip et al., 2007), still
needs to be determined and need continuous research efforts to
focus on this area especially for the recovery of nutrient depleted
degraded soils.
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)
2 Phosphorous (P)
3 Potassium (K)
4 Iron (Fe)
5 Aggregate formation
Diazotrophs fix N2 as ammonia through their metabolic
process. Bacteria from family Rhizobiaceae living in the soil
infect plant root to form nodules and fix N in this structure
through complex enzymes system.
P solubilization or availability is enhanced by P mineralization
as well as well as production of siderophores and organic acids
in the soil.
Bacteria release various types of organic acids to solubilize K in
the soil through various processes such as acidolysis, chelation,
complexolysis and exchange reactions.
Production of siderophores which has affinity to chelate and
solubilize iron from mineral or organic compounds.
Produce peripheral slime polymers and decompose organic
material to form organo-mineral products that are associated
with soil particles to form aggregates.
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 fix
N.
Increase P bioavailability through mineralization in soil,
mycelial transport, P solubilization by siderophores, N
assimilation and CO2 release.
Influence K mobilization through mycelial transport as well as
by K solubilization process that involves the release of H+ , CO2
and organic acid such as citrate, malate and oxalate.
Translocate Fe from mineral to organic soil horizon for
decomposition and mineralization, and release chelator
(siderophores) for Fe translocation in soil.
Hyphal network entrap soil particle and forces them together.
Production of mucilages, polysaccharides and extracellular
compounds as well as soil proteins such as glomalin and
hydrophobins.

3.1.1. How do fungi influence N2 fixation?
As discussed above, fungi indirectly affects N2 fixation through
bacteria present in mycelia. During this process, fungi translocate
carbon and P from the plant roots to the associated bacteria for N2
fixation. In this regard Paul and Kucey (1981) observed a symbiotic
association of bacteria and fungi with legumes, which may indi-
cate a competition between these microbes for carbon provided by
legume roots. However, this competition is masked by the associ-
ation of AM fungi with Rhizobia who provides a high amount of P
for nitrogenase enzyme complex (Puppi et al., 1994). The enhanced
N2 fixation ability of the bacteria through AM association is dete-
riorated by the depletion of P zone in mycorrhizosphere. AM fungi
also provide plant derived carbon to increase the potential ability
of non-symbiotic N2 fixer such as Herbaspirillum and Azospirillum.
During this association, AM fungi decrease the total amount of sugar
and enhance nitrogenous compounds in mycorrhizosphere (Jones
and Oburger, 2011). The changes occurred in this region strengthen
the carbon limitation of N2 fixer over other microorganisms which
could limit their performance to fix N2 (Veresoglou et al., 2012).
On the other hand, non-symbiotic N2 fixer are versatile organisms
which possess the ability to adapt the carbon and N limiting condi-
tions (Blaha and Schrank, 2003). Their performance is not affected
by the changes that occur in rhizosphere due to AM fungi colo-
nization (Veresoglou et al., 2012). Therefore, it is not always true
that AM fungi association with plant and rhizobia would be benefi-
cial for long term recovery of degraded land as proposed by Chaer
et al. (2011). In such condition, carbon limitation could be replen-
ished by organic amendments in addition to the synergistic effect
of co-inoculants such as N-fixing bacteria and AM fungi. Such phe-
nomenon needs to be further investigated for sustainable recovery
of degraded soils. In this regard, efforts are done to figure out the
sole inoculation of N-fixing bacteria or AM fungi with organic fer-
tilizers and obtained encouraging results for the rehabilitation of
degraded land under semi-arid environment (Medina et al., 2010;
Mengual et al., 2014a; Mengual et al., 2014b).
3.2. Phosphorus mobilization
Phosphorus (P) is another essential and growth-limiting nutri-
ent in agro-ecosystems (Smil, 2000). However, this limitation could
be fulfilled by external inputs to the soil in the form of organic
as well as synthetic fertilizers (Fig. 2). The later form of fertilizer
is formulated from the rock phosphate reserves. Therefore, many
researchers are concerned about rapid diminution of the world’s
P reserves due to continuous mining for P (Cordell et al., 2009;
van Vuuren et al., 2010). Recently, there is a contradiction in views
regarding the availability of world P reserves. Simulation studies
suggested that global P production will reach to maximum by 2033
(Cordell et al., 2009) while other researchers had concluded that
almost 50% of the currently available P reserves will be mined by
2100 (van Vuuren et al., 2010).
In most of the agricultural soils (productive or degraded), huge
reserves of inorganic or organic P are present in immobilized or
unavailable form. Fonte et al. (2014) observed no difference in
total P in degraded and productive pasture, however in this study,
organic P was 40% higher in latter pasture soil. They explained this
by showing the presence of higher inorganic P in degraded than
productive pasture which was strongly adsorbed or occluded in
this soil. In fact, inorganic P is highly reactive with some metal com-
plexes such as iron, aluminum and calcium (Fig. 2), which lead to
75–90% 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 available
to 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 well
as any applied insoluble finely ground rock P. Such type of inocula
are now termed as P-mobilizing microbes (Owen et al., 2015) rather
than previously referred as phosphate-solubilizing microorgan-
isms (Rodrıı́guez and Fraga, 1999; Rodriguez et al., 2004; Dastager
et al., 2010; Jones and Oburger, 2011). As these inocula do not only
solubilize P, but they also mobilize its organic form through miner-
alization (enzymatic hydrolysis) and facilitate the translocation of
phosphate (Owen et al., 2015); Fig. 2). Microbes are responsible for
mobilizing the soil P unavailable for plants through their direct and
indirect effects. In direct processes, (i) microbes solubilize P by low-
ering the pH (through proton extrusion) of external medium and
producing 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 and
Oburger, 2011; Zhang et al., 2014). Hydroxyl and carboxyl groups
of 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 through
which indirect mobilization of P can be carried out by these inoc-
ula: (i) Microbes release CO2 during respiration which is dissolved
in 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 the
available P (Illmer and Schinner, 1992) (iii) P solubilizing microbes
 M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41
Fig. 2. An overview of the mechanism used by bacteria and fungi to mobilize nutrients (P, K and Fe) in the soil.
to enhance nutrient bioavailability. Specifies primary intermediary steps.
have the ability to remove and assimilate phosphate from the soil
in order to re-establish the P equilibrium, in this way they stimulate
the indirect dissolution of Ca–P (Halvorson et al., 1990); (Fig. 2).
3.3. Potassium
Potassium (K) is another vital nutrient and considered as a key
parameter of soil fertility and plant growth. In most of the soils, K
is present in very small amount ranging from 0.04 to 3%. Despite
being in limited amount, 98% of this K is bound within phyllosili-
cates structure (Shelobolina et al., 2014). This is the layer of silicate
minerals found in silt and clay fractions of the soil. The remaining
2% exists in soil solution or on exchange sites to become avail-
able for the plants (Sparks and Huang, 1985). Hence, soil fertility is
decreased due to low availability of this nutrient which is normally
fulfilled by commercial fertilizer (i.e., KCl), thus elevating the input
cost of the farmers. Recently, few microbial strains were isolated
who had an ability to oxidize in the first step Fe2+ from primary
phyllosilicates mineral in such a way that they release iron and
K from these minerals (Shelobolina et al., 2014). Bacterial inoc-
ula (Neutrophillic lithotrophs) utilize structural Fe2+ in biotite as an
electron donor for their metabolism in order to produce energy
and oxidize biotite (Shelobolina et al., 2014). The microbes which
oxidized biotite (Fe2+ -bearing mica) include Bradyrhizobium japon-
icum, Cupriavidus necator, Ralstonia solanacearum, Dechloromonas
agitate, and Nocardioides sp . In addition to this, Sheng and He
(2006) suggested that inoculation of B. edaphicus NBT strains and
its mutants increase the production of citric, oxalic, tartaric, suc-
cinic, and ␣-ketogluconic acid. These acids lead to K mobilization
from K-containing minerals (e.g. mica, biotite, kaolinite and smec-
tite) and chelation of silicon ions (Han and Lee, 2005; Sheng and
He, 2006).
3.3.1. Fungi and K mobilization
In addition to bacterial strains, mineral form of K is solubilized by
fungi through releasing organic acid anions which mainly includes
citrate, malate and oxalate (Meena et al., 2014). According to Wu
et al. (2005), K uptake was increased in corn crop after inoculation
of G. mosseae (now, Funneliformis mosseae) and G. intraradices (now,
31
Indicates processes carried out by microbial inocula
Specifies secondary intermediary steps. Microbial inoculum.
Rhizoglomus intraradices) (Sieverding et al., 2014). In degraded soil
(acidic), K solubilization was higher than calcium and magnesium
after inoculation of AM fungi compared to un-inoculated control
(Clark et al., 1999). Inoculation of Aspergillus terreus and Aspergillus
niger increased the K level in soil solution by solubilizing K from
insoluble 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 K
mobilization?
The major processes involved in mobilizing K are acidolysis and
complexolysis exchange reactions (Uroz et al., 2009). During aci-
dolysis, soil inocula such as bacteria or fungi decrease the local pH
by producing succinic, citric, gluconic, ␣-ketogluconic and oxalic
acids (Fig. 2). Production of protons (H+ ) and organic acids anions
not only enhances the chelation of cations which are bound to K but
also 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 chelate
Al and Si cations associated with K minerals and by doing so they
also enhance the exchangeable K in soil solution (Römheld and
Kirkby, 2010). Consequently, microbes not only synthesize but also
discharge 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 structural
unavailable forms of K compounds in to soil solution resulting an
increased 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 earth
and predominantly exists in nature in ferric (Fe3+ ) form. It is
considered as one of the key micronutrient for soil fertility and
is also needed by all kind of living organisms. It is sparingly
 32
Table 2
Examples 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)
√ √ √ √

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

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 Rodrıı́guez 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.
 M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41
Table 3
Examples of various fungal strains involved in improving soil fertility and structural parameters.
No. Fungi
1 Rhizophagus irregularis
2 Agaricus lilaceps
3 Paraglomus occultum
4 Glomus mosseae
5 Laccaria bicolor, L.laccata, Lactarius theiogalus, Paxillus involutus and Suillus bovinus
6 R. intraradices, G.aggregatum, G.viscosum, Claroideoglomus etunicatum, C.claroideum
7 G. mosseae and G. intraradices
8 Aspergillus terreus and A. niger
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
microbes in aerated soil. Moreover, in soil, ferrous (Fe2+ ) is oxi-
dized to Fe3+ thereby forming insoluble compounds and leaving a
very low amount of iron for microbial or plant assimilation (Ma,
2005). Therefore, to fulfill iron requirement for normal growth,
tough competition exists among bacteria, fungi and plant in the rhi-
zosphere. In such circumstances, some strains of bacteria (Sharma
et al., 2003; Vansuyt et al., 2007) synthesize low-molecular mass
proteins known as siderophores. These molecules have high affin-
ity to chelate (Machuca et al., 2007; Miethke and Marahiel, 2007)
and solubilize iron from mineral or organic compounds. Generally,
siderophores have high affinity to form complexes with Fe3+ (1:1).
Uptake of the complexes by the cell membrane of both Gram posi-
tive and negative bacteria reduces Fe3+ –Fe2+ . Later cell membrane
expel these ions from the siderophores into the cell (Boukhalfa and
Crumbliss, 2002) by linking its inner and outer membranes, a mech-
anism called “gating”. In this way siderophores solubilize iron from
unavailable minerals or organic compounds in iron limited con-
dition (Indiragandhi et al., 2008). Additionally, bacteria produce
extracellular siderophores which deprive pathogenic organisms
produced under Fe limited condition and form complexes with
other heavy metals (Zn, Pb, In, Cu, Ga, Cd and Al) (Schalk et al.,
2011) and radionuclides including U and Np (Kiss and Farkas, 1998;
Neubauer et al., 2000). Presence of such heavy metals encourages
the bacteria to produce siderophores which chelate the metal to
increase Fe availability in the rhizosphere of these soils (Wang et al.,
2002). Such bacteria play a vital role in elevating heavy metal con-
centration by phytoextraction through enhancing the activity of
antioxidants. Hence, siderophores produced by microbial inocula
also play a key role in alleviating the stresses imposed on plants
through heavy metals.
3.5. Interaction between bacteria and fungi inocula to improve
nutrient bioavailability in soil
Fungi and bacterial inocula interact with plant roots to improve
nutrient availability in soil for plant uptake (Glick, 1995; Smith and
Read, 2010; Prakamhang et al., 2015); Tables 2 and 3). For this pur-
pose, the co-inoculation between bacteria–bacteria, fungi–fungi or
bacteria–fungi species is also significantly acknowledged in recent
studies (Tytova et al., 2013; Leifheit et al., 2015; Nguyen and Bruns,
2015; Ortiz et al., 2015; Prakamhang et al., 2015). In these inter-
actions, mycelium of AM fungi release carbon compounds which
will act as energy source for soil microorganisms in the mycor-
rhizosphere, though the carbon products are in small amount than
already present in rhizosphere (Andrade et al., 1997). Similarly, bac-
teria also exude carbon compounds which increase the AM fungi
hyphal growth and its root colonization (Barea et al., 2005). Dur-
ing the interaction among Rhizobia, AM fungi and legume, AM
fungi enhance the growth and yield of legume by providing water
and nutrients, especially P which increases Rhizobium N2 fixation
33
N P K OM AF/GP AS Reference
√ √ √
– – – Leifheit et al., (2015)
√ √
– – – – Caesar–TonThat et al., (2013)
√ √ √
– – – Wu et al., (2014)
√ √ √ √ √
– Xu et al., (2015)
√ √
– – – – (Zhang et al., 2014)
√ √ √
– – – Bona et al., (2014)
√
– – – – – Wu et al., (2005)
√
– – – – – Prajapati et al., (2012)
through influencing energy production pathways (Minerdi et al.,
2001; Mortimer et al., 2008). Bacteria enhance P availability for
uptake of AM fungi and plant through phosphatase enzyme and
organic acid production in the soil (Owen et al., 2015). Thus, their
co-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, N
fixation, P, K and Fe mobilization (Fig. 2). For instant, effect of
co-inoculation of plant growth promoting bacteria and Bradyrhi-
zobium increase the soybean seed yield up to 44% per hectare than
their lone (single) inoculant form (Prakamhang et al., 2015). Sim-
ilarly co-inoculation of B. thuringiensis or Ps. putida with AM fungi
increase P by 44 and 35% in Trifolium repens respectively, while K
content was increased by 128 and 285%, than their lone inocula-
tion (Oritz et al., 2015; Table 4). Hence, interactions among soil
microbes in the soil rhizosphere positively affect soil fertility and
provide highly valuable ecosystem services. Therefore use of these
inocula can be exploited in order to increase yield, reduce chemical
inputs, and develop an efficient form of sustainable fertilizer man-
agement in agro-ecosystems (Bhattacharjee et al., 2008; Nguyen
and 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 in
influencing the bioavailability of various nutrients (Table 4); there-
fore co-inoculation of microbes could prove to be more beneficial
in recovery of degraded soil. However, some strains of bacteria
or fungi can possess more than one mechanism and may prove
to withstand under water limited or nutrient depleted condition,
therefore could be potential option for reinstating the lost functions
of 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 organic
matter through intensive soil management practices and land use
changes (Oldeman et al., 1990; Montgomery, 2007). However, soil
structure plays a central role in crops management and thus agri-
cultural ecosystems sustainability (Rillig et al., 2002). This can
be defined as size, shape and three dimensional arrangements
of organic or mineral complexes (aggregates) and pores in such
a manner that affect pore continuation, water infiltration and
water 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 together
through organic, inorganic or chemical forces in order to form
aggregates. 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 soil
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).
Soil structure is mainly articulated by the degree of aggregate
stability (Amezketa, 1999). Organic matter is one of the main
agents in aggregate formation and stabilization. Therefore, increas-
ing organic matter in soil is very vital for the rehabilitation of
degraded soils. Other factors involved in this process are persistent
cementing agents like humic acid that stabilizes microaggregates
and polysaccharides derived from plants as well as microbes. Fun-
gal hyphae, plant roots and bacteria are temporary binding agents
in the formation and stabilization of macroaggregates (Tang et al.,
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
wetting and drying cycles (Sun et al., 2014). Soil aggregation sta-
bility is a multifaceted process and is an indicator of many aspects
of soil structure including erosion, soil water regime and nutrient
availability. The stability of aggregates is controlled by soil phys-
ical, chemical, and/or microbial community properties and plant
roots (Zadorova et al., 2011; Graf and Frei, 2013; Pérès et al., 2013).
Among soil microbes, AM Fungi symbionts typically represent a
major force in stabilizing macroaggregates than bacteria (Tang
et al., 2011; Leifheit et al., 2014) which stabilize microaggregates.
4.1. Bacteria and soil aggregation
Influence of bacteria on soil aggregation is dependent on soil tex-
ture and nutrient availability (Degens, 1997). They reside mainly in
the form of individual cells, microcolonies or biofilms in the aque-
ous solution within the pores of soil aggregates, thus ensuring that
they may attach to surfaces of microaggregates (Fig. 3). Bacteria
decompose organic material to form organo-mineral products that
are associated with soil particles to form stable microaagregates
(2–20 ␮m diameter) (Tisdall, 1994). These small microaggregates
are in turn bound by bacterial and saprophytic fungi products to
form slightly larger aggregates (20–250 ␮m diameter) (Miller and
Jastrow, 2000). Moreover, during bacterial growth, extracellular
polymeric substances are produced in the form of peripheral slime
polymers into soil solution (Aspiras et al., 1971); Fig. 3). These are
negatively charged polysaccharides, polyuronic and amino acids
with adhesive properties capable of making bond between clay par-
ticles in order to form aggregates (Tang et al., 2011; Caesar-Tonthat
et 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; Bedini
et al., 2009; Peng et al., 2013) as well as it can modify the mor-
phological structures and biochemical nature of host plants (Borie
et al., 2008) including its roots and rhizosphere. Additionally, AM
Fungi can also alter soil microbes in its surrounding environment as
well as the rhizosphere of host plant which are probably involved
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
Bedini et al. (2013), mean weight diameter of aggregate (an indica-
tor of stability) is strongly correlated with hyphal length of fungi but
weakly 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 in
soil. They also observed that this group of fungi plays an important
role in stabilization of soil aggregates.
 M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41
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
Mycelium of AM fungi impacts soil aggregation through com-
plicated direct and indirect mechanisms which are strongly
interdependent (Fig. 3). In direct mechanism, hyphal network of
AM, ectomycorrhizal, saprophytic and others fungi entraps soil
particles and forces them together (Tisdall, 1994; Peng et al.,
2013; Zheng et al., 2014). On the other hand, Chenu et al., 2002
reported that hyphal network aligns soil particles along its expand-
ing hyphae to form aggregates (Fig. 3). During indirect mechanism,
mycelium exudes glomalin, hydrophobins and related soil proteins
as well as mucilages, polysaccharides and extracellular compound
into the soil (Rillig et al., 2006; Caesar-TonThat et al., 2013). Accord-
ing to Driver et al. (2005), about 80% of glomalin protein is bound
in hyphal wall which helps in transporting nutrients and water for
AM fungi. It protects the fungal hyphae and lipid rich spores from
drought and microbial attack which form clumps of soil aggre-
gate through decomposed hyphae, glomalin protein fused with
minerals (sand, silt and clay) and organic matter (Borie et al.,
2008). Glomalin is hydrophobic protein which contributes to the
hydrophobicity of soil aggregates. In addition to this, the glue-like
nature of glomalin also helps in the initiation and stabilization of
aggregates (Miller and Jastrow, 2000) and may act as adhesive
agent to bind soil particles together (Chenu, 1989; Wright and
Upadhyaya, 1996). Saprotrophic fungi produce extracellular exu-
dates that promote water stable aggregates (Ambriz et al., 2010).
Similarly extracellular mucilages like polysaccharides exuded by
basidiomycetes and Trichocomaceae bind the soil particles into
aggregates and increased their stability (Caesar-TonThat, 2002;
Daynes et al., 2012). Some species of ectomycorrhizal fungi exudes
hydrophobic compounds which are important in exploring large
distance in the soil for transporting nutrients and water for fungi
(Agerer, 2001) Fig. 3). Hydrophobins are small proteins, considered
to affect soil wettability and water repellency from the aggregates
(Diehl, 2013). By exuding hydrophobic compounds, fungi tend to
increase hydrophobic soil organic matter that can avoid breakage
of dry soil aggregates in the rewetting process and thus creat-
ing more water stable aggregates (Six et al., 2004). This could be
in line with more recent findings of Xu et al. (2015) who had
reported that AM fungi increased soil organic carbon which was
positively related to normalize mean weight diameter of aggre-
gates. They suggested that increase in soil organic carbon by AM
fungi could be a mechanism through which fungi improve soil
structure.
35
4.3. Interaction between fungi and bacteria to improve soil
aggregation and their stability
Fungi influence microbial communities in the soil rhizosphere
through many ways (as discussed above) and the interaction facili-
tated by AM fungi leads to changes in the turnover and distribution
of soil aggregates. However, these changes are arbitrated, and the
prominence of these changes to soil aggregation and other medi-
ated processes are poorly defined (Rillig et al., 2006). Fungi deposit
organic compounds in the mycosphere through mycelium which
act 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-TonThat
et al. (2013) Pseudomonas fluorescens and Stenotrophomonas mal-
tophilia isolated from Agaricus lilaceps fruiting body binds soil more
than 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 surrounding
microbes. 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, as
well as their functional attributes vary within aggregate sizes (Chen
et al., 2015; Gupta and Germida, 2015).
In addition to rhizospheres microbes, AM fungi can potentially
influence soil aggregation by affecting plant communities, plant
roots (individual host), and soil fauna such as earthworms, termites
or ants. These biota are considered to be key soil engineers (details
about 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 plant
roots binds and stabilize macroaggregates (>250 ␮m) in particular
(Tisdall and Oades, 1982) whereas microaggregates (<250 ␮m) are
stabilized 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 or
processes which are driven by different set of traits epitomized in
different species (Rillig et al., 2015). Therefore, to reinstate the soil
structure in degraded soils, it would be unwise to rely only on one
or two components. Instead, the process is cumulative involving
various factors such as plant root, soil biota (microbes and animal)
and organic matter that could be enhanced by activities of soil life
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
Organic amendments such as animal manure (solid cattle
manure and slurry), compost and crop residues could play an
important role in enhancing the fertility of degraded soil. These
amendments increase the organic matter and thus influence the
soil life by providing them a source of food. Enhancing soil
organic matter is the most important step to rehabilitate the
strongly degraded land. Since this parameter play a significance
role in increasing the capability of the ecosystem to support the
more diverse and complex community composition, formation of
soil aggregates, maintenance of soil structure, fertility and water
holding capacity (Tiessen et al., 1994; Kononova, 2013). Rashid
et al. (2014a) observed that continuous application of solid cat-
tle manure increased organic matter, N, pH, microbial biomass and
soil fauna in sandy soil compared to that of slurry manure fertiliza-
tion. Application of urban refuse increased soil microbial activities
as well as AM fungal diversity in degraded soil of semi-arid region
(del Mar Alguacil et al., 2009). In addition to these studies, use of
poultry manure and wheat straw in degraded soil of Himalayan
region increased organic matter content, hydraulic conductivity,
aggregate stability, N, P, K, carbon sequestration and pH compared
to urea or unfertilized control (Khaliq and Abbasi, 2015). Combine
application of solid cattle manure and chemical fertilizer increased
soil organic matter, N, microbial biomass and the crop productivity
and reduce the decreasing stock of soil carbon (Srinivasarao et al.,
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
carbon sink. Moreover, application of bio-solids and vegetative yard
compost increased fungal biomass and enzymatic activity in indus-
trial degraded soil compared to un-amended control during the first
year of application however enzymatic activity was declined in the
second year (Carlson et al., 2015). Therefore, such findings could
restrict the lone use of organic amendments for the nutrient man-
agement of degraded soil and may urge researcher to think of more
mixed management option rather than simple solutions.
5.1. Bacterial and fungal inocula to reinstate the fertility of
degraded land
Bacterial and fungal inocula play an important role in the
restoration of degraded soil. Singh, (2014) reported that cyanobac-
teria fix atmosphere N2 in degraded soils and release extracellular
polysaccharides, which are metabolized by the associated soil
microorganisms. In addition, other bioactive compounds produced
by these bacteria positively influence soil fertility, decrease soil
pathogens and therefore improve crop growth (Singh, 2014). Bio-
logical N2 fixing bacteria encourage the growth and persistence
of other soil microbial groups in the rhizosphere by providing
N (Seneviratne et al., 2008). Similarly bacteria exude extracel-
lular polysaccharides that promote soil aggregations (Degens,
1997). Bacterial strains also mobilize the fixed or unavailable
P, K and Fe in the soil (discussed in various sections). In addi-
tion to this, bacterial inocula also produce phyto-hormones
(Auxin/Indole Acetic Acid) which improve plant defense against
various pathogens (Lugtenberg and Kamilova, 2009; Ahemad
and Kibret, 2014; Goswami et al., 2015). These inocula also
produce aminocyclopropane-1-carboxylate deaminase that pro-
motes the root elongation, shoot growth, and enhances rhizobial
nodulation as well as N, P and K uptake in various crops
(Nadeem et al., 2009; Glick, 2012, 2015; Goswami et al., 2015).
Plant growth promoting bacteria induce systemic resistance
and produce antifungal metabolites (HCN, phenazines, pyrrolni-
trin, 2,4-diacetylphloroglucinol, pyoluteorin, viscosinamide and
tensin). Hence they act as biocontrol agent in various diseases and
environmental stresses (Bhattacharyya and Jha, 2012; Goswami
et al., 2015). Ectomycorrhizal and AM fungi also increase the soil
nutrient and water transport through soil exploration by their
hyphal 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 can
mobilize N, P, K, Fe and other nutrients in the soil and transfer these
nutrients to the host plants (Smith and Read, 2010) through translo-
cation process by hyphal network (Fig. 2). AM fungi can reduce N
and P losses (Asghari and Cavagnaro, 2012) through leaching and
N2 O emission (Bender et al., 2015) and enhanced nutrient intercep-
tion of AM fungi rooting systems. Due to these activities, microbial
inocula drive nutrient cycling and at the same time also deter-
mined whether these nutrients are made available to plants. By
doing so, these microbial inocula can achieve satisfactory results in
the restoration of degraded soil. Seneviratne et al. (2011) observed
that application of biofilm based fertilizers developed from N2 fixer
bacteria increased N2 fixation and soil organic carbon. Hence, these
fertilizers stimulated the ecosystem functioning and help in achiev-
ing sustainable restoration of degraded agricultural soil within few
months in tropics. Microbial communities present in these biofilm
based fertilizers substantially enhanced the microbial biodiversity
which leads to sustainability of agro-ecosystem and environment
(Seneviratne et al., 2011).
5.2. Application of bacterial and fungal inocula with organic
amendments to reinstate the fertility of degraded land
Few researchers use combination of bacteria or fungi inocula
with organic amendments to reinstate one or few parameters of
degraded soil in controlled experiments and obtained promising
results (Medina et al., 2004; Mengual et al., 2014a,b; Leifheit et al.,
2015). For instance, Leifheit et al. (2015) used fungal inoculum with
organic residues to increase soil aggregation and their stability in
pot experiment while Mengual et al., (2014a,b) found increase in
soil P availability, total N and other microbiological and biochemical
parameters with co-application of bacterial inocula and composted
sugar beet in small field assay. Recently it was found that combined
effect of bacterial and fungal inocula and cover crops increased P
mobilization and soil organic matter in subtropical red soils dur-
ing a time duration of six months (Cui et al., 2015). They found
that 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 enhanced
this parameter by 5.4% (18.94 ± 1.03 vs. 17.97 ± 1.02, P > 0.05) from
P. natatu. Moreover, in this study moderately labile organic P was
also increased from control (302.8 ± 4 vs. 272.5 ± 9.2, P = 0.05). This
form of P strongly influence the phosphomonoesterase enzyme
activity (Cui et al., 2015). Hydrolytic enzymes released by soil inoc-
ulants are main drivers of carbon, N and P cycling hence they
play a key role in hastening the nutrients cycling in soils for plant
growth (Burns et al., 2013). Thus, a combined application of organic
amendments, cover crops, fungal and bacterial inocula could be
a good approach for the sustainable restoration of degraded soil
which is not considered yet under field conditions. In above discus-
sion, it had been highlighted that direct application and symbiotic
interactions of bacterial and fungal inocula with crops and organic
fertilizers could be used as an emerging tool for restoring degraded
lands. Therefore, adequate selection for the combined application
of diverse communities of bacteria, fungi and organic fertilizers
could be a key to restore and reinstate the degraded ecosystems.
 M.I. Rashid et al. / Microbiological Research 183 (2016) 26–41
5.3. Gaps in current approaches and way forward to restore the
degraded land
It is apparent from the above discussion that microbial inoc-
ula are one of the valuable bio-resources that could be helpful in
restoring degraded lands. However, most of the researchers use
lone bacterium or fungal strain in their experiments that can par-
tially result in the reported discrepancies at field scale (Table 4). The
reasons for lower response than co-inoculation could be that single
microbial inoculum is not likely to be active as it faces competition
of resources from indigenous microorganisms in order to survive in
soil environment (Singh, 2014, 2015). To make the inocula success-
ful under field condition, it could be fascinating to test whether the
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
or fungal inocula may create synergistic effects (Singh, 2015) while
organic manures can meet their nutrient demands to make them
successful under field conditions. These associative interactions
could be successful and may play a crucial role in restoring the pro-
ductivity of degraded soils. However, field experiments are lacking
evidence to support these hypotheses. Singh (2015) proposed that
successful restoration of degraded soil using microbes required a
combined knowledge on microbiology, ecology, biochemical mech-
anisms and field engineering. Moreover, most of the soil functions
i.e. organic matter stabilization, decomposition, nutrient mobiliza-
tion, translocation and mineralization, and aggregate formation
and stability are carried by microbes. To attain the sustainable pro-
ductivity in agro-ecosystems, the aforementioned soil functions
have not been fully explored due to complex microbial diversity
in these soil ecosystems. Therefore, it is very important to further
explore unidentified microorganisms that can live in competitive
environment under field conditions and help to increase the soil
fertility and productivity of degraded soils in order to meet the
increasing global food demand and at the same time environmental
sustainability.
6. Future considerations
Bacteria and fungi are integral part of soil microbial commu-
nity. These microbes play a vital role in the restoration of degraded
soils through fertility enhancement by affecting nutrients cycles
as well improvement in soil structure. Regardless of encouraging
evidences on the application of microbial inocula for improving
nutrient bio-availability and soil aggregation, still many aspects
need to be explored for further studies which are as follows:
1. Many studies have revealed that the application of single bacte-
rial or fungal inoculum or their co-inoculation to soil improves
its fertility and aggregation. In most cases, co-inoculation per-
formed better than their sole/lone counterpart (Table 4) but
there are still certain aspects that require serious attention such
as evaluation of these approaches under field conditions. Major-
ity of experimental studies are carried out in laboratory or in
the pots under controlled conditions, therefore performance or
adaptability of these microorganisms under field condition may
differ significantly. Under natural field conditions, both biotic
and abiotic factors are not controlled and the competition for
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
and productivity of degraded land. However, adequate selec-
tion of microbial inocula to enhance their synergistic effect has
not gained much attention from the scientific community. This
needs to be further explored by the researchers.
37
3. To achieve sustainability in crop production, studies regarding
microbial inocula should focus more on nutrient cycling (fix-
ation, mobilization, translocation, leaching losses and gaseous
emissions) rather than only single fate of the nutrient. There-
fore the focus of future studies must be based on the processes
to understand the influence of microbial inocula on nutrient
cycling.
4. Bacterial and fungal inocula could be successfully employed in
reinstating fertility of degraded soils. However, their applica-
tions would consider the inherent limitations of these inocula
and figure out the best strains of both bacteria and AM fungi who
can establish a long-lasting association to improve the fertility
and structure of such soils.
7. Conclusions
In the coming decades, land degradation will be major threat to
the food security. Therefore most important issue is how to feed the
increasing population of the world where about 84% of agricultural
land 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 degraded
soil 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 of
enhancing nutrient bioavailability and improving soil aggregation.
Hence they could be used in reinstating the fertility of degraded
soils. Understanding the mechanisms of microbial inocula in the
provision or mobilization of nutrients in degraded land is a key
for their success in field applications. Although exact mechanisms
through which bacteria and fungi achieve these benefits in such
soils are not fully understood, however it is becoming clearer that
few or all traits of these microbes can allow them to perform their
associated functions. To this end, a better understanding on the
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
practices for improving the fertility and crop production capac-
ity of degraded soils. Use of single inoculum or co-inoculation of
bacteria-bacteria, bacteria-fungi or fungi–fungi could not always
be very fruitful for the reclamation of degraded soils. In fact, lone
or dual strains with distinct functions are less active and could
not survive in nutrient deficient soil environment due to compe-
tition of resources for their survival. However, addition of organic
fertilizer with co-inoculation of bacterial and fungal strains could
have a potential for restoration of degraded soils because organic
matter can fulfill the nutrient demand while bacteria and fungi
can create synergistic effect for nutrient acquisition as well as soil
aggregate formation and stabilization. Hence, inoculation of bacte-
ria and fungi with organic fertilizers can reduce the excessive use
of 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 this
study is to realize that for complete restoration of degraded soils, a
combinatorial mixture of management practices is necessary. This
includes inoculation of soil biota (microbes and animal) in addition
to organic fertilizers, plant roots and other associated factor like
growing of cover crops.
Acknowledgments
This review was supported by the Ministry of Higher Education,
Kingdom of Saudi Arabia, Centre of Excellence in Environmental
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
of Information Technology, Vehari, Pakistan.
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