Climate Change and Environmental Sustainability (October 2016) 4(2): 137-149
DOI:
REVIEW ARTICLE
Role of Beneficial Soil Microbes in Sustainable Agriculture and
Environmental Management
Jitendra Mishra1 Jai Prakash2 Naveen Kumar Arora3*
Abstract Rapidly increasing human population is expected
to make food security a big issue in the future. Agriculture
is facing severe challenges of land degradation, lesser
productivity and susceptibility towards a biotic and biotic
stresses. Sustainability in the agricultural sector is proving
a formidable task because the current trend involves
excessive use of chemical fertilisers and pesticides. Besides
these, anthropogenic activities such as urbanisation and
industrialisation are generating more waste that is posing a
severe threat to the ecosystems. Various approaches were
being tried to eradicate waste and restore ecosystems, but
the success was limited. Beneficial soil microbes (BSMs)
are identified as suitable candidates that may help in the
sustainable management of the environment. These
microorganisms possess several mechanisms that can be
exploited at the commercial level in developing
biotechnology for solving the key environmental issues.
Beneficial microbe-based products currently used in
agroecosystems have shown are markable success. Their
proper use in agroecosystems is changing the scenario of
present-day agriculture. In the future, utilisation of such
microbes in the clean-up of pollutants, waste eradication and
combating climate change can provide substantial aid in on-
going-greener campaign towards environmental
sustainability. In this review, we have summarised the role
of BSMs particularly the plant-growth-promoting bacteria
and fungi in sustainable agriculture and also addressed their
role in the management of environmental problems.
Keywords Beneficial soil microbes, Pollutants, Climate
change, Agroecosystems, Sustainability, Agriculture, Plant
Growth Promoting Rhizobacteria
1. Introduction
The human population is increasing very rapidly and
creating excessive pressure on the existing land area for food,
, Research Scholars, 3Head of Department, Department of Environmental Microbiology, School for Environmental Sciences, Babasaheb
1 2
Bhimrao Ambedkar (Central) University, Lucknow-226025, Uttar Pradesh, India.
*Corresponding author e-mail id: nkarora_net@rediffmail.com
fuel and raw materials. To supply the demand, agriculture
practices are using intensive amounts of chemical fertilisers
and pesticides which has resulted in land degradation and
loss of biodiversity (Carsten and Mathis, 2014). In many
developing countries, agriculture plays a vital role in the
economic development and also provides self-employment
(Gindling and Newhouse, 2012). According to an estimate,
it was found that developing countries such as India,
Pakistan, Bangladesh, Iran, Afghanistan, Nepal, Sri Lanka
and Bhutan are losing crops, equivalent to at least, US$10
billion annually due to land degradation (Lal et al.,
2010).Several factors have been reported by the researchers,
which are responsible for degradation of soils. Among them,
anthropogenic activities are directly involved in the land
degradation process. The result of land degradation, may be
exhaustion, salinisation and desertification of soil (Kesavan
and Swaminathan, 2008). Many technological inventions are
being carried out for the improvement of crop productivity,
but still, we are not in a position to fulfil the global demand
for food. Microbes associated with plants can be used to
overcome the problems related to soil salinity, fertility,
degradation and habitat loss. Soil contains diverse organisms
like bacteria, archaea, fungi, algae, insects, annelids and other
invertebrates which show an intimate relation to each other
and with plants (Glick, 2010). Among them, microbial
entities are unique as they are directly involved in increasing
soil fertility, plant growth promotion and lowering biotic
and abiotic stresses by various mechanisms which are known
as BSMs. BSMs enhance the plant growth by nutrient uptake,
form complex soil matrix and help in plant defence response
by secretion of various metabolites. In addition, BSMs can
show tolerance towards adverse environmental conditions
such as salt stress, drought stress, weed infestation, nutrient
deficiency and heavy metal contamination. Since past few
years, researchers have found that soil microbes play
beneficial and harmful roles in the soil ecosystem. However,
138 Climate Change and Environmental Sustainability (October 2016) 4(2): 137-149
BSMs gained much importance not only for their plant
growth promoting attributes but also for role in
decomposition of organic wastes, detoxification of toxic
substances such as pesticides and alleviation soil stresses
(Aislabie and Deslippe, 2013; Ma et al., 2016). This review
explains the role of BSMs, particularly plant growth
promoting rhizobacteria (PGPR), plant growth promoting
fungi (PGPF)including mycorrhiza and cyanobacteria in
sustainable agriculture. In addition to this, how the
application of BSMs can be utilised in a sustainability of
environment is also discussed.
2. Beneficial Soil Microbes (BSMs)
The soil is naturally occurring physical covering of the
earth surface and represents the interface of three material
states: solids (geological and dead biological materials),
liquids (water) and gases (air in soil pores) and considered
as the foundation of all terrestrial ecosystems (Aislabie and
Deslippe, 2013). In the captivity of soil, vast diversity of
microbes such as bacteria, archaea and fungi are critically
engaged with each other and involved in ecosystem
functioning. According to an estimate, one gram of soil may
contain 10101011 bacteria, 6,00050,000 bacterial species
and up to 200 m fungal hyphae (Blackwell, 2011) and
majority of them are considered to be beneficial for plants
Figure 1. Plant-growth-promotion mechanism by PGPR
as well as soils. Their direct association with plants root
causes mineral uptake from the soil, decompose organic
matter, acquisition of nutrient and also help in plant growth
promotion as well as suppression of phytopathogens
(Nihorimbere et al., 2011). Soil also contains harmful
microbes which invade or parasitise plants and reducing
productivity. The presence of BSMs makes soil healthy and
growth suppressive for harmful microbes.
3. Plant Growth Promoting Rhizo-bacteria (PGPR)
PGPR are potential microbes that facilitate plant growth
either directly or indirectly by colonising the plant root
(Kloepper and Schroth, 1978; Lugtenberg and Kamilova,
2009; Mishra and Arora, 2012; Ahemad and Kibret, 2014;
Goswami et al., 2016). These soil bacteria have the ability
to colonise roots and stimulate plant growth. PGPR species
belong to many different genera such as Azoarcus,
Azospirillum, Rhizobium, Azotobacter, Arthrobacter,
Bacillus, Clostridium, Enterobacter, Gluconoacetobacter,
Pseudomonas and Serratia (Cheng, 2009; Mishra and Arora,
2012; Arora, 2015). During recent past, much research has
been carried out to reveal the mechanisms of plantmicrobe
interactions (Beneduzi et al., 2012). Besides, PGPR may
affect the plant growth directly or indirectly (Figure 1). Direct
growth promotion involves the production of
Climate Change and Environmental Sustainability (October 2016) 4(2): 137-149
phytohormones, fixation of atmospheric nitrogen (N2),
synthesising iron chelators known as siderophores,
solubilising inorganic minerals such as phosphorus (P),
potassium (K) and zinc (Zn), making them more readily
available for plant growth (Ahemad and Kibret, 2014).
Indirect role can be seen in the form of their growth inhibition
activity against phytopathogens by one of the several
mechanisms such as antibiotic or antifungal metabolite(s)
production, depletion of iron from the rhizosphere, induced
systemic resistance (ISR), production of fungal cell wall lytic
enzymes and competition for binding site(s) on the roots
(Vejan et al., 2016). In addition, PGPR are also recognised
as potential microbes that can protect the plant from various
environmental stresses in normal as well as stressed
environment (Khare and Arora, 2011; Kang et al., 2014).
There is an ample literature which describes the effective
role of PGPR in sustainable agriculture (Ahemad and Kibret,
2014; Arora and Mishra, 2016). Although initially the role
of PGPR was explored only for enhancing the crop
productivity, several studies are now confirming that PGPR
play a pivotal role in proper functioning of the agro-
ecosystems (Cheng, 2009). Research also showed that they
can be used in the restoration of degraded land, improving
the quality of soil, reducing the environmental pollutants
from the soils and also combating climate changes (Kuiper
et al., 2004).
4. Plant Growth Promoting Fungi (PGPF)
Soil contains a wide variety of beneficial and pathogenic
fungi that affect plants at all stages. According to an estimate,
1.5 million fungal species may be present in natural
ecosystems, but only 510% have been described formally
(Laughlin and Stevens, 2012). Soil fungi typically make up
the largest percentage of the biomass of the soil communities
(Robertson and Groffman, 2007) and viewed as major
contributors to soil nutrient cycling processes including
nitrogen mineralisation, immobilisation and transformation
(Selim et al., 2012). Plantfungi interaction starts when roots
release some specific chemical compound(s) that act as
nutrient sources or defence against pathogenic microbes. For
example, compounds derived from cortical and epidermal
cells stimulate the proliferation of fungi outside, on the
surface and inside the roots whereas release of some phenolic
compounds inhibits the growth of entomopathogenic fungi
(Selim et al., 2012). The fungal species such as Alternaria
spp., Aspergillus spp., Aureobasidium spp., Candida spp.,
Cladosporium spp., Paecilomyces spp., Phoma spp.,
Penicillium spp. and Sporobolomyces spp. are present in soil
which are agriculturally important and remained subject of
considerable research over many years.
The mycorrhizal symbiotic association has been shown
by 80% of all terrestrial plants (Gaur and Kaushik, 2011;
139
Marcel et al., 2015). Beneficial effects of mycorrhizae are
amenable to natural ecosystem where intervention activities
are very less (Lehman et al., 2015). There are two types of
mycorrhiza, ectomycorrhizae and endomycorrhizae, and
both are important for sustainable agriculture (Smith and
Read, 2008). Although on the basis of fungal diversity and
with plant association, endomycorrhiza is further subdivided
(Presto et al., 2013). One of the endomycorrhizasis
arbuscular mycorrhiza (AM) formerly known as vesicular
arbuscular mycorrhiza (VAM) which shows anobligate
relationship with plants. According to Parniske (2008), plants
can enhance 420% of their photosynthate to support AM
fungi, which is equivalent to the consumption of roughly 5
billion tonnes of carbon per year by arbuscular mycorrhizal
fungi (AMF). AM fungi show a symbiotic relationship with
host plants and form spore in the soil with the ability to
germinate under harsh environmental condition(s) and help
in alleviating abiotic stresses in the plant (Becerra et al.,
2014). AM fungi play an important role in soil structuring
by formation of a network of extraradical hyphae which
holds soil particles together. The most significant effect of
AM fungi is to enhance the uptake of phosphorus in their
host plant (Aggarwal et al., 2011). AM fungi also interact
with nitrogen-fixing bacteria and phosphate-solubilising
bacteria (PSB) which synergistically help in plant growth
and development. The dual inoculation treatment (AM fungi
and bacteria) has significantly increased the biomass and
nitrogen as well as phosphorus uptake in plant tissues (Puppi
et al., 1994). Research showed that huge amounts of bacteria
and fungi are found associated with AMF. For example, some
AM hyphae adhere rhizobia and pseudomonads which
appear to be vehicles for root colonisation (Bianciotto et
al., 2000). Ample literature is available on the tripartite
symbiosis of legumemycorrhizaRhizobium (Barea, 2000)
and their role in improvement of nodulation and N2 fixation.
Nair et al. (2001) reported that mycorrhizal infection is
beneficial for growth of cowpea (Vigna unguiculata L.).
Recently, the interaction of mycorrhiza with PGPR has also
been tested for improving crop productivity under stressful
environments (Nadeem et al., 2014).Thus, mycorrhizal fungi
play crucial role to benefit the host plant mainly through
acquisition of nutrients from soil and also protects from biotic
and abiotic stresses.
5. Cyanobacteria
Cyanobacteria are photosynthetic prokaryotes and
ubiquitous in nature. They are found commonly in lakes,
ponds, springs, wetlands, streams and rivers. Besides,
cyanobacteria are also important component of soils (Singh
et al., 2016). Fritsch (1907) first noticed the abundance of
cyanobacteria in rice-fields and further De (1939) showed
their importance in the maintenance of rice-field fertility due
140 Climate Change and Environmental Sustainability (October 2016) 4(2): 137-149
to N2 fixation and considered them as a natural biofertiliser
(Song et al., 2005; Sahu et al., 2012). The free-living
cyanobacteria or symbiotic have been used for sustainable
agriculture. According to Smil (1999), free-living
cyanobacteria or symbiotic cyanobacteria (like with water
fern Azolla) fix 46 Tg N2 annually. Efficient nitrogen-fixing
cyanobacteria like Nostoclinkia, Anabaena variabilis,
Aulosirafertilisima, Calothrix sp., Tolypothrix sp. and
Scytonema sp. were identified from various agro-ecological
regions and utilised for rice production (Prasad and Prasad,
2001). Although the use of cyanobacteria and their utility in
rice field has been in practice since long but recently their
use with other crops has also been tested. For example, an
ammonia-excreting mutant of A. variabilis has shown growth
enhancement of wheat crop (Spiller et al., 1993).
Cyanobacteria not only contribute in global N2 supply but
reports also indicate them to be involved in phytohormones
production in free living and symbiotic associations. For
example, Nostoc, Chlorogloeopsis, Calothrix, Plectonema,
Anabaena, Cylindrospermum and Anabaenopsis have shown
indole acetic acid (IAA) production in rice and wheat
rhizosphere (Karthikeyan et al., 2007; Manjunath et al.,
2011). Cyanobacteria also help in soil formation process by
excreting extracellular polysaccharides, peptides and lipids
during their growth in the soil (Kaushik, 2014; Rosa and
Philippis, 2015). Some reports are indicating that
cyanobacteria can grow successfully in the saline soil where
most plants (except halophytes) fail to grow and help in
increasing fertility of such soils (Singh and Dhar, 2010).
6. Role of BSMs in Sustainable Agriculture
6.1 Bio-Fertilisers
Bio-fertilisers are those substances that contain living
microorganisms that colonise the rhizosphere of the plants
and increase the supply or availability of primary nutrients
and/or growth stimulus to the target crop (Bhattacharjee and
Dey, 2014). They are applied in the agricultural fields as
replacement to conventional fertilisers. Bio-fertilisers are
gaining impetus due to the maintenance of soil health,
minimising environmental pollution and cut down on the
use of chemicals in the agriculture (Saeed et al., 2015).
Various beneficial microbes have been used as bio-fertilisers
for different crops (Table 1). PGPRs, particularly N2 fixing,
phosphate and potassium solubilisers are recommended as
a sustainable solution to improve plant-nutrient uptake and
crop production (Bhattacharjee and Dey, 2014). According
to an estimate, farmers usually need to apply at least 100 kg
of N2 per hectare (Deaker et al., 2004), whereas the use
efficiency is generally below 40%, meaning that most applied
fertiliser either washes out or is lost to the atmosphere.
Biological nitrogen fixation (BNF) is in the order of 100
and 290 million tons of N2/year and provides N without any
costin terrestrial ecosystems (Cleveland et al., 1999), out of
which 4048 million tons/year is fixed by crops (Jenkinson,
2001). According to an estimate, cyanobacteria in symbiotic
association contribute 780kgN2/ha/year, free-living 15
kgN2/ha/year and associative (endophytic) bacteria 36kgN2/
ha/year (Elkan, 1992). It has been observed that cereal crops
may obtain up to 30% of their N2 from BNF when fertilised
with high rate of phosphorus and potassium as well as with
microelements (Pedraza, 2008; Mmbaga et al., 2014).
Rhizobial inoculants have been applied to legume crops for
over 120 years as bio-fertilisers (Marks et al., 2007). Many
countries are promoting the use of rhizobial inoculants for
nitrogen uptake; for example, in Brazil, application of
rhizobial inoculants in soybean crop provides N2 with a value
equivalent to US$ 7 billion for fertilisers (Hungria et al.,
2007). Rennie and Hynes (1997) stated that Canada has a
substantial market of Rhizobium inoculant products. In some
studies, Rhizobium inoculation also showed the biocontrol
potential against soil-borne phytopathogenic fungi (Arora
et al., 2001). Among non-symbiotic N2-fixing bacteria, the
most extensively studied genus is Azospirillum. In addition
to increasing plant-nitrogen content, it also improves the
plant growth by production of phytohormones such as
auxins, cytokinins and gibberellins (Steenhoudt and
Vanderleyden, 2000). Recently, legumes and their
association with rhizobia and AMF have also been
recognised for better nitrogen and phosphate uptake by plants
and gaining importance in agroecosystems (Kaschuk et al.,
2010). This tripartite association was not only effective in
nodule formation, AM colonisation, nitrogen fixation but
also supported the faba bean plants growth under alkalinity
stress (Abd-Alla et al., 2014).
PSB and AMF are reported since long to solubilise
insoluble phosphates and help in increasing yield of several
crops (Hameeda et al., 2000; Fernandez et al., 2007; Shahab
et al., 2009). Studies indicate that application of rock
phosphate in conjunction with PSB could reduce 50% cost
of addition of chemical fertilisers (Yazdani et al., 2009).
There are several publications demonstrating that PSB-based
inoculation increases P content of sugarcane (Sundara et al.,
2002), mung bean (Vikram et al., 2008), maize (Oliveira et
al., 2009), rice (Sarkar et al., 2012) and wheat (Sarker et
al., 2014). PGPR are known to have the capability of iron
uptake in low-iron condition and enhance plant productivity
(Sahaet al., 2015). Bio-fertilisers for solubilising non-
exchangeable K are also in practice in some agro ecosystem
(Sangeeth and Suseela, 2015).
In plants, zinc (Zn) is regarded as an essential
micronutrient (Sauchelli, 1969) but only very little amount
remains available to plant, due to its transformation to
different chemical forms (Brown et al., 1962; Mandal and
Climate Change and Environmental Sustainability (October 2016) 4(2): 137-149 141

Table 1. Characteristics of some BSM-based bio-fertilisers

Types of Name of Microbe Description References

Bio-fertilisers Used

Nitrogen fixers Rhizobium spp. Rhizobium is known for their ability to fix atmospheric nitrogen Baset Mia and
in symbiotic association with plants forming nodules in roots Shamsuddin (2010)
Azospirillum spp. It is free-living and non-symbiotic nitrogen fixer, beneficial to a Bashan (1993)
wide array of crops covering cereals, millets, vegetables, cotton
and sugarcane
Azotobacter spp. Rapidly grow in various agricultural soils fixes high level of Siddiqui et al. (2014)
nitrogen
Cyanobacteria Some cyanobacteria have terminally differentiated, specialised Kaushik (2014)
structures called heterocyst and considered as photodiazotrophs.
Their presence in rice fields provided aid in nitrogen uptake
Azolla spp. This water fern has asymbiotic relation with blue, green algae Carrapico et al. (2000)
and can help rice or other crops cultivation
Phosphate Pseudomonas spp., PSB and Mycorrhiza can help in improving uptake of an insoluble Duarah et al. (2011)
solubilisers Bacillus spp., form of phosphate to plants in different ways
Rhizobium spp.,
Burkholderia spp.
and Mycorrhiza
Zinc solubilisers Bacillus spp., Solubilise zinc compounds like zinc oxide (ZnO), zinc carbonate Ahemad and Kibret
Pseudomonas spp. (ZnCO3) and zinc sulphide (ZnS) and may reduce the rate of (2014)
costly zinc sulphate
Potassium Bacillus spp., Solubilise potassium, present in the insoluble form of rocks and Shanware et al. (2014)
solubilisers Burkholderia spp., silicate minerals
Pseudomonas spp.
Phytohormones Pseudomonas, Produce phytohormones such as auxins, cytokinins, gibberellins Ahemad and Kibret
producers Bacillus, Rhizobium, and ethylene can affect cell proliferation in the root architecture (2014)
Burkholderia and by overproduction of lateral roots and root hairs with a
Mycorrhiza subsequent increase in nutrient and water uptake. The enzyme
1-aminocyclopropane-1 carboxylic acid (ACC) is a pre-requisite
for ethylene production, catalysed by ACC oxidase

Mandal, 1987). Various studies have indicated that the
release of insoluble and fixed forms of Zn by zinc
solubilising bacteria is an important aspect of increasing soil-
Zn availability through the production and excretion of
organic acids (Bhupinder et al., 2005). PGPF have been
extensively studied for solubilisation of insoluble zinc
compounds both in vitro and in vivo conditions. However,
some genera of PGPR such as Acinetobacter, Bacillus,
Gluconacetobacter and Pseudomonas have been reported
to solubilise insoluble zinc.
6.2 Biopesticides
About 40% of the potential global crop yield is destroyed
by pests (invertebrates, plant pathogens and weeds) before
it is harvested and another 20% is destroyed post-harvest
(Bailey et al., 2010). However, for sustainable agriculture,
use of chemical-based pesticides should be relinquished
because of their negative impact on the environment.
Workers around the world are now using biopesticides and
trying to minimise the use of conventional chemical
pesticides. Biopesticides are pesticides derived from natural
materials such as animals, plants, bacteria and minerals
(USEPA, 2008). Worldwide, approximately 1400
biopesticide products are being sold (Marrone, 2007) and
their number is increasing day by day. For the global status
of biopesticide use and regulation as well as availability,
one can see review by Mishra et al. (2015) and Arora et al.
(2016). Microbial pesticides are also known as biocontrol
agents (BCAs). Microbes as biopesticides offer the
advantage of higher selectivity and lower or no toxicity in
comparison with conventional chemical pesticides (Mac
Gregor, 2006). BCAs can be grouped into three broad
categories, namely bacterial, fungal and viral. Among the
most widely used bacterial pesticides are the strains of
Bacillus thuringiensis (Bt), accounting for approximately
90% of the biopesticide market in the USA (Chattopadhyay
et al., 2004), several species of Pseudomonas showed
biocontrol potential against phytopathogens (Arora et al.,
2008; Kang et al., 2014). For example, biopesticides
containing Pseudomonas fluorescence and Pseudomonas
142 Climate Change and Environmental Sustainability (October 2016) 4(2): 137-149

syringae have been used at large scale now (Arora et al.,
2015). Fungal biopesticides include Trichoderma harzianum,
used against plant pathogens, which is an antagonist of
several soil-borne fungi such as Rhizoctonia, Pythium,
Fusarium and other phytopathogens (Hartmann et al., 2008).
Baevuria bassiana and Metarhizium anisopliae are naturally
occurring entomopathogenic fungi considered as good BCA
and infect-sucking pests including Nezara viridula L. (green
vegetable bug) and Creontiades sp. (green and brown mirids)
(Sosa-Gomez and Moscardi, 1998). Baculovirus is the main
viral BCA that is commercially used for designing phage
pesticides. As of 2010, over 24 baculovirus species have
been reported to be registered for use in insectpest
management throughout the world (Kabaluk et al., 2010).
Currently, most commonly used microbial biopesticides are
of biofungicides (Trichoderma, Pseudomonas and Bacillus),
bioherbicides (Phytophthora) and bioinsecticides (Bt)
(Gupta and Dikshit, 2010). Data indicates that among the
biopesticide market for all crop types, bacterial biopesticides
claim about 74%, fungal biopesticides, about 10%, viral
biopesticides, 5%, predator biopesticides, 8% and other
biopesticides, 3% (Thakore, 2006). Some major
biopesticides used in agroecosystems are mentioned in Table
2.

Table 2. Some of the BSMs-containing biopesticides used in agroecosystem

S. No. Types of BSMs General or Commercial Name Target Organism

PGPR
1. B. thuringiensis subsp. aizawai Turex Lepidoptera pests
2. B. thuringiensis subsp. israelensis VectoBac Lepidopteran pests
3. B. thuringiensis subsp. kurstaki Dipel WP, Batik, Lepidoptera pests
4. Bacillus subtilis Kodiak Fusarium, Pythium and Rhizoctonia
5. Bacillus amyloliquefaciens Taegro Fusarium and Rhizoctonia wilt diseases
6. Bacillus licheniformis EcoGuard Downy mildew, Fusarium wilt
7. Bacillus pumilus Sonata Seedling diseases
8. Bacillus popilliae Milky Spore Powder Japanese beetle grubs
9. Pseudomonas chlororaphis At-Eze Soil and seed-borne fungi
10. Pseudomonas syringae Bio-Save 10LP Postharvest diseases
11. Pseudomonas. aureofaciens Spot-Less Turf fungal diseases
12. Pseudomonas fluorescens Biomonas, Esvin Bacterial wilt, root rot
13. Pseudomonas alcaligenes Not Known Locusts, grasshoppers
14. Pseudomonas aureofaciens Spot-Less Turf fungal diseases
15. Pseudomonas resinovorans Agriphage Insect pest control
16. Pseudomonas syringae AgriPhage Bacterial speck
17. Agrobacterium radiobacter NoGall Crown gall disease
18. Pantoea agglomerans BlightBan C9-1 Fire blight

PGPF
1. Beauveria bassiana Naturalis L, Botanigard Thrips, whitefly and mites
2. Metarhizium anisopliae Biomagic, Biomet Coleoptera and lepidopteran insect
3. Trichoderma harzianum Biozim, Phalada 105 Soil-borne pathogens
4. Trichoderma viride Monitor, Trichoguard, Soil-borne pathogens
5. Verticillium lecanii ABTEC, Ecocil Whitefly, coffee green bug,
6. Pythium oligandrum Polyversum Root rots
7. Trichoderma gamsii Remedier, Bioten Soil-borne pathogens
8. Trichoderma polysporum Binab T Soil and foliar diseases
9. Paecilomyces fumosoroseus Preferal WG Greenhouse whiteflies
10. Alternaria destruens Smolder Herbicide dodder
11. Candida oleophila NEXY Postharvest disease
12. Aspergillus flavus Afla-guard Aspergillus flavus producing aflatoxin
Source: Modified from Mishra et al. (2015)
Climate Change and Environmental Sustainability (October 2016) 4(2): 137-149
6.3 Bioherbicides
Bioherbicides are used to control the herbs/weeds which
are harmful to crops, in a sustainable manner (Harding and
Raizada, 2015). Mainly fungi-based bioherbicides got
success as the potential of bacteria is hardly explored in weed
control and viruses prove difficult to handle on the ground
of their host specificity and dependence on vectors
(Charudattan, 2005). Different trade names have
commercialised the rust fungus, Puccinia canaliculata and
Chondrostereum purpureum-based bioherbicides. Plant-
pathogenic bacteria Xanthomonas campestris pv. poannua
(Xcp) and P. syringaepv. tagetis (Pst) have also been used
in the formulations of bioherbicides (Johnson et al., 1996).
7. Role of BSMs in Environmental Management
Whole world is coping with various environmental
issues which are difficult to handle. Environmental pollution
due to excessive use of fossil fuels, waste generation from
different anthropogenic activities, land degradation and
climate change due to greenhouse gas emissions are major
ones. All problems are generally man-made and caused by
increasing population, industrialisation, urbanisation and
deforestation. Research has now, proven the role of BSMs
in remediation of environmental problems and identified
them as potential tools to attain the goal of sustainable
environment (Satyanarayana et al., 2012). In this section,
we discuss various roles of BSMs that could be effectively
incorporated for the management of environmental
problems.
7.1 Bioremediation
Bioremediation is a process for the clean-up of
hazardous compounds present in the environment by
application of biological agents (Glick, 2010). Biological
agents including microbes (microremediation), plants
(phytoremediation) or both (rhizoremediation) are used for
bioremediation purposes. In situ bioremediation involves
stimulation of indigenous microbial population to degrade
contaminants and remained in practice for a long time. Plant-
associated bacteria including endophytes and PGPR produce
a range of natural products, thus enhancing the
bioremediation of environmental soils (Gianfreda and Rao,
2004). It has been reported that BSMs such as Azospirillum
lipoferum, Enterobacter cloacae, Pseudomonas putida and
Pseudomonas fluorescens have potential to remediate
polycyclic aromatic hydrocarbons (PAHs), total petroleum
hydrocarbons (TPHs) and trichloroethylene (TCE)
contaminated soils (Zhuang et al., 2007; Glick, 2010).
Mining industry releases a variety of heavy metals such as
zinc, lead, copper and cadmium in soil, presenting a major
threat to pollute the environment. The conventional
techniques for treatment of metal-containing wastes such as
143
thermal processes, physical separation, electrochemical
methods, washing, stabilisation/solidification and burial for
clean-up of contaminated soils are too expensive and have
harmful effects on the environment (Dermont et al., 2008;
Khan et al., 2015). Studies indicate that the BSMs can act
directly on organic pollutants (Kuiper et al., 2004). Some
plants and microbes have developed the unique capability
of heavy-metal tolerance (Reichman, 2014) and being
utilised in remediation of metals (Table 3).
Microbe-assisted phytoremediation has also been
investigated in the laboratory, greenhouse and field for
detoxification of organic contaminants (Zhuang et al., 2007;
Glick, 2010; Ukaegbu-Obi and Mbakwem-Aniebo, 2014).
Some studies also describe that PGPR screened for
siderophore production, complexed other metals as well. For
example, siderophore producing Alcaligene ssp. STC1 and
P. aeruginosa RZS3 strains were found to remove various
heavy-metal ions at batch scale and bioremediation potential
of these strains were found to be superior over the chemical
ion chelators (Sayyed and Patel, 2011). Besides, several
reports are indicating that siderophoreby PGPR can also be
utilised in themetal uptake of gallium, chromium and thorium
(Kazy et al., 2009). AM fungi, genus Glomus, Scutellospora,
Acaulospora and Gigaspora, are of much importance in
metal transformation (Khan et al., 2014). Recently, research
on biosurfactants for metal uptake have been carried out
(Thavasi et al., 2011) and findings suggest that P. aeruginosa
rhamnolipid containing biosurfactants complexes metal such
as lead, cadmium and zinc could be used in metal
contaminated soils (Pacwa-Plociniczak et al., 2011).
Rhizoremediation is also an effective tool in which
rhizospheric microbes collectively contribute in degradation
of pollutants (Anderson et al., 1993). Studies indicate that
degradation of herbicides and pesticides via rhizoremediation
not only improved the soil but also prevented plants from
deleterious effects of these compounds (Kuiper et al., 2004).
7.2 Biodegradation
Biodegradation is a process by which organic
compounds are transformed into microbial biomass and other
simpler compounds ultimately releasing water and CO2 into
the atmosphere (Ramana and Singh, 2000). Microorganisms
cause structural changes or complete degradation of the target
molecule by both chemical and physical processes (Wirn-
Lehr et al., 2002). Due to the high catabolic diversity of
BSMs, they can degrade, transform or accumulate various
compounds including hydrocarbons (oil), polychlorinated
biphenyls (PCBs), polyaromatic hydrocarbons (PAHs)and
radionuclides (Glick, 2010). BSMs including PGPR and
PGPF are known to produce a variety of contaminant-
degrading enzymes such as peroxidases, dioxygenases, P450
monooxygenases, laccases, phosphatases, dehalogenases,
144 Climate Change and Environmental Sustainability (October 2016) 4(2): 137-149

Table 3. Bioremediation of heavy metals by PGPR

Plants PGPR Metals Experiments Results References

Pisum sativum Rhizobium sp., Chromium Glasshouse conditions Improved the nitrogen Soni et al. (2014)
Microbacterium (VI) (54%) concentration in
sp. the plants
Decreased Chromium
toxicity
Scripusucronatus Brevundimonas Mercury Green house Increase phytoremediation
diminuta, Decrease toxicity in soil
Alcaligenes
faecalis
Helianthus anus Bradyrhizobium Arsenic Pot studies Excess of plant biomass Yavar et al. (2014)
and Triticuma japonicum Growth in high arsenic
estivum CB1809 concentration
Brassica napus Bacillus Lead Under field conditions Soil pollution decreased Reichman (2014)
megaterium Total dry-matter yield of
plants
Prosopis juliflora, Bacillus, Chromium Green house condition Improve the efficiency of Wani and Khan
Lolium mltiforum Staphylococcus, Cadmium, phytoremediation (2012)
Aerococcus Cupper, Lead Tolerate high conc. of
and Zinc Chromium (up to 3,000
mg/l)

nitrilases and nitroreductases (Chaudhry et al., 2005).
Several VAM fungi produce xylanases, mannases and other
enzyme complexes that may aid in the partial degradation
of hazardous compounds (Singh, 2006). PGPR are good
root-colonising bacteria that effectively colonise root vicinity
and utilise root exudates as sole carbon and energy source
and participate in the degradation of organic contaminants
as well by direct metabolism or co- metabolism (Wirn-Lehr
et al., 2002). Plant-growth-promoting Pseudomonas and
Brevibacillus were reported in degradation or removal of
petroleum contaminated soils (Zhuang et al., 2007). Penta
choro phenol (PCP) degrading bacteria belonging to PGPR
groups have also been discovered (Marihal et al., 2009).
Chlorpyrifos pesticide degrading bacteria include the
Providencia stuartii isolated from agricultural soil (Rani et
al., 2008). Certain PGPF such as Mucoralternans, Fusarium
oxysporum and Trichoderma virideare known to degrade
dichloro diphenyl trichloroethane (DDT) (Patil et al., 1970).
White-rot fungi mainly Phanerochaete chrysosporium and
Trametes versicolor are used as model organisms in lignin
biodegradation (Mouginrubi, 2002). A number of other
white-rot fungi that is Pleurotuso streatus, T. versicolor,
Bjerkandera adusta, Lentinula edodes, Irpex lacteus,
Agaricus bisporus, Pleurotustuber regium and Pleurotus
pulmonarius can also degrade persistent xenobiotic
compounds (Singh, 2006).
8. Stress Management
With increasing human interference and rapidly
changing climatic conditions, abiotic stresses such as high
temperature, flood, prolonged drought and frost are expected
to intensify in near future. As abiotic stress factors adversely
affect crop productivity, therefore, their rapidly increasing
impact on agriculture and food production is a serious
concern. Several researches have suggested that BSMs
possess the outstanding capability to mitigate the negative
impact of abiotic stress factors on plants (Yang et al., 2009).
Soil microorganisms, particularly those present in rhizosp
here enhance tolerance of plants towards abiotic stresses by
increasing nutrient acquisition, improving soil texture,
moisture content and organic matter in soil, as well as
inducing certain biochemical, physiological and molecular
changes in plants which support their growth during
unfavourable conditions (Venkategowda and Kumar, 2015).
Rhizospheric microbial communities change in response to
stress conditions and are dominated by tolerant communities
which are adapted to the modifications through complex
regulatory processes at the molecular level (Sharma et al.,
2013). One important mechanism by which soil
microorganisms facilitate the growth of plants under stress
conditions is the production of the enzyme 1-
aminocyclopropane-1-carboxylate (ACC) deaminase. This
enzyme decomposes 1-aminocyclopropane-1-carboxylic
acid, an ethylene precursor in plants, therefore, lowers the
ethylene production in plants and enhances resistance
towards stress conditions (Glick, 2005). In response to
drought stress, some microbial species produce
exopolysaccharides (EPS) which help in osmoregulation,
synthesise ACC-deaminase, IAA and proline. Pantoea
agglomerans, Rhizobium spp. and Pseudomonas spp. are
Climate Change and Environmental Sustainability (October 2016) 4(2): 137-149
known for production of EPS, which improves soil texture
by forming macroaggregates and by increasing water holding
capacity of soil (Tewari and Arora, 2014; Naseem and Bano,
2014). Stress-tolerant fungi hold much promise in a
sustainable environment. Their stress-adapted enzymes, as
well as the genes that code for those enzymes, may be
especially important. For example, drought-tolerant species
of Aspergillus, Aureobasidium, Chrysosporium,
Cladosporium, Fusarium, Geotrichum, Myrothecium,
Oidiodendron, Paecilomyces, Penicillium, Rhizopus,
Scopulariopsis, Trichoderma, Wallemia and Xeromyces have
been isolated from arid regions, and their survival is a matter
of interest. Several eco-physiological studies investigating
the role of AM fungi in the management of drought stress
show that they may alter the rate of water movement into
the host plants and protect them from the detrimental effects
of water-deficit conditions (Ruiz-Lozano, 2003). Similarly,
Azospirillum sp. and AM fungi also support plant growth
by increasing water circulation, whereas Pseudomonas
mendocina and Glomus intraradices enhanced antioxidant
status in plants and Bacillus megaterium and Glomu ssp.,
produce IAA and proline to support plant growth during
stress conditions (Grover et al., 2010).
It has been estimated that changing climatic conditions
will result into loss of arable land by up to 50% by the year
2050 (Munn, 2002), and soil will be more prone to salinity
as well. The use of PGPR for saline-soil reclamation is
cheaper and effective method. It has been studied that when
PGPR are inoculated in rhizoshphere of plants growing in
saline conditions results in improved plant growth as well
as nutrient availability (Dimkpa et al., 2009) and protection
against phytopathogens (Tewari and Arora, 2014).
9. Combating Climate Change
Climate change is one of the major threats to the
environment and also affecting the soil microbial function
and diversity [Intergovernmental Panel on Climate Change
(IPCC), 2007]. According to an estimate, global soils are
supposed to contain twice as much carbon as in the
atmosphere, making them one of the largest sinks for
atmospheric CO2 and organic carbon (Jenkinson et al., 1991).
Soil-microbe area is fundamental determinants of global
carbon pool (Brady and Weil, 2008; Schlesinger and
Andrews, 2000). Hence, small changes in global carbon flux
can have a significant impact on atmospheric carbon dioxide
(Schlesinger and Andrews, 2000). For example, as the human
intervention began, soils are estimated to have lost 40 to 90
billion tons of carbon from stored ~2,000 billion tons of
organic carbon (Lal, 1999). As the BSMs are bestowed with
several mechanisms that are essential for their survival in
altered climate conditions, they have received considerable
scientific attention around the globe. Various workers are
exploring the application method of BSMs that could be used
145
in mitigation of anthropogenic climate changes. The use of
PGPR can be a very good method to combat the impact of
climate change and emphasis should be on development of
multifunctional strains that can be utilised in stressed
agroecosystems (Naseem and Bano, 2014). PGPRs like
Achromobacter, Azotobacter, Azospirillum, Acetobacter,
Bacillus, Chryseobacterium, Flavobacterium, Enterococcus,
Klebsiella, Pseudomonas, Rhizobium, Serratia and
Paenibacillus are now being used for conflicting and
ameliorating drought and salinity stresses in diverse habitats
(Arora et al., 2012). Recently in a study Nie et al. (2015)
ascertained the role of BSMs in increased plant productivity
and decreased microbial respiratory C loss under elevated
CO2 concentration. One of the better options which helps in
combating climate change are mycorrhizae because they
have evolved in response to changes in global climate and
developed various mechanisms for supplying the possible
higher nutrient demands of the host plant under changing
climate conditions (Staddon, 2005). Soil organic matter and
carbon-credit generation can be sustainably maintained by
use of BSM (Bellarby et al., 2008). Use of chemical
fertilisers are responsible for increasing emissions of
greenhouse gases such as CO2, CH4 and nitric oxide (N2O),
whereas BSMs used as inoculants in agriculture play a key
role in minimising dependence on chemical fertilisers thus
helping in combating climate change (Adesemoye et al.,
2009).
10. Challenges and Future Prospects
The excessive use of chemical fertilisers and pesticides
and various other anthropogenic activities are deliberately
destroying agroecosystems and the balance of our planet.
As a consequence, loss of soil fertility and crop productivity
has generated awareness among agriculturists, and their
consent of using BSMs in agroecosystems have gained
momentum for enhancing plant productivity and soil quality
in its native form. Soil microbes are endowed with various
mechanisms to work as efficient candidates in the field of
sustainable agriculture and environment management. It has
been analysed that in properly managed-agriculture systems,
BSMs can act as bio-fertilisers, biocontrol agents and soil
improvers. BSMs containing inoculum may replace synthetic
chemicals, which result in environmental hazards and pose
a serious toxicological threat to the ecosystem. Beneficial
microbes used in biocontrol tend to have high-target
specificity and are environment-friendly. The role of BSMs
in environmental sustainability can be expanded if we get
success in finding some unrevealed concepts related to their
ecology, population dynamics and functionality over a range
of environments. As in near future, the global human
population will increase further and in this situation,
agricultural sector would be dependent even more on BSMs
to increase agricultural production in an eco-friendly manner.
146 Climate Change and Environmental Sustainability (October 2016) 4(2): 137-149
11. Conclusion
Use of BSMs in sustainable agriculture and environment
management offers countless benefits. Their utilisation in
the form of bio-fertilisers and biopesticides is becoming
popular and providing substantial aid to the agroecosystems.
Their capability to survive in harsh environmental conditions
makes them efficient candidates in different types of stress
management, whereas their catabolic diversity can be used
in the removal of recalcitrant pollutants. Our understanding
of the BSMs response in agroecosystems is increasing, and
their potentially significant effects on environment
restoration are also strengthening and collectively helping
to obtain the goal of sustainable development. Impact of
climate change particularly in the agriculture sector may be
also minimised by the application of BSMs. However, with
climate change perspective, effective use of BSMs requires
more investigations and it has been realised that elucidation
of mechanisms involved in their interaction with plants in
extreme conditions may provide better chance of their vast
application in environmental sustainability.
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