Chapter 16

Can Bacillus Species Enhance Nutrient

Availability in Agricultural Soils?

Vijay Singh Meena, B.R. Maurya, Sunita Kumari Meena,

Rajesh Kumar Meena, Ashok Kumar, J.P. Verma, and N.P. Singh

Abstract One major challenge for the twenty-first century will be the production of
sufficient food for the global human population. The negative impacts on soil–plant–
microbes–environmental sustainability due to injudicious use of chemical fertilizer,
pesticide, insecticide, etc. by the unaware farmers deteriorate soil and environment
quality. One possible way to use efficient soil microorganisms to remediate nutrient
deficiency in agricultural soils and other plant growth-promoting (PGP) activities

V.S. Meena (*)

Department of Soil Science and Agricultural Chemistry, Institute of Agricultural Sciences,
Banaras Hindu University, Varanasi 221005, Uttar Pradesh, India
ICAR-Vivekananda Institute of Hill Agriculture,
Almora 263601, Uttarkhand, India
e-mail: vijayssac.bhu@gmail.com; vijay.meena@icar.gov.in
B.R. Maurya • A. Kumar
Department of Soil Science and Agricultural Chemistry, Institute of Agricultural Sciences,
Banaras Hindu University, Varanasi 221005, Uttar Pradesh, India
S.K. Meena (*)
Division of Soil Science and Agricultural Chemistry, Indian Agriculture Research Institute,
ICAR, New Delhi 110012, India
Department of Soil Science and Agricultural Chemistry, Institute of Agricultural Sciences,
Banaras Hindu University, Varanasi 221005, Uttar Pradesh, India
e-mail: sumeena66@gmail.com
R.K. Meena
Department of Plant Sciences, School of Life Sciences, University of Hyderabad,
Hyderabad 500046, Telangana, India
Department of Genetics and Plant Breeding, Institute of Agricultural Sciences, Banaras Hindu
University, Varanasi 221005, Uttar Pradesh, India
J.P. Verma
Institute of Environment and Sustainable Development, Banaras Hindu University,
Varanasi 221005, Uttar Pradesh, India
N.P. Singh
Department of Genetics and Plant Breeding, Institute of Agricultural Sciences, Banaras Hindu
University, Varanasi 221005, Uttar Pradesh, India

© Springer International Publishing AG 2016 367

M.T. Islam et al. (eds.), Bacilli and Agrobiotechnology,
DOI 10.1007/978-3-319-44409-3_16
368 V.S. Meena et al.

that can be of help for plant growth and development. The Bacillus species is one the
most dominant rhizospheric bacterial/rhizobacteria species like Bacillus subtilis, B.
cereus, B. thuringiensis, B. pumilus, B. megaterium, etc. that can help enhance the
plant growth and development by different mechanisms, which PGPR can inhibit
phytopathogens is the production of hydrogen cyanide (HCN) and/or fungal cell wall
degrading enzymes, e.g., chitinase and ß-1,3-glucanase. Direct plant growth promo-
tion includes symbiotic and non-symbiotic PGPR which function through produc-
tion of plant hormones such as auxins, cytokinins, gibberellins, ethylene, and abscisic
acid. Mitigate the challenge by adopting eco-friendly crop production practices.
Some Bacillus species function as a sink for 1-­aminocyclopropane-­1-carboxylate
(ACC), the immediate precursor of ethylene in higher plants, by hydrolyzing it into
α-ketobutyrate and ammonia and in this way promote root growth by lowering indig-
enous ethylene levels in the micro-rhizo environment. Bacillus species also help in
solubilization of mineral phosphates, potassium, zinc, and other nutrients; rhizobac-
teria retain more soil organic N and other nutrients in the soil–plant system, thus
reducing the need for fertilizers and enhancing release of the nutrients from indige-
nous or mineral sources, enhancing the economic and environmental sustainability.

Keywords Bacillus spp. • Mineral solubilization • Rhizosphere • Fe sequestration

• Efficient microorganisms • Nutrient uptake

16.1 Introduction

World food insecurity is a chronic problem and is likely to worsen with climate change
and rapid population growth. It is largely due to poor yields of the cereal, pulse, and
millet crops caused by factors including soil–plant–environment system. The world’s
population is assumed to increase from ~7 billion now to 8.3 billion in 2025. The
world will need 70–100 % more food by 2050 (Godfray et al. 2010). The increasing
human population is placing greater pressure on soil and water resources and threat-
ening our ability to produce sufficient food, feed, and fiber. As a result, there is a
growing consensus within our global community that the protection of natural
resources and implementation of environmentally and economically sound agricul-
ture practices is of the utmost priority (Ahmad et al. 2016; Bahadur et al. 2016a).
Nowadays world agriculture is facing new challenges in which ecological and
molecular approaches are being integrated to achieve higher crop yields while mini-
mizing negative impacts on the environment. In this direction, enhancing nutrient
availability, plant growth and yield, and plant multi-stress resistances are key strate-
gies. Root-, soil-, and plant-associated eco-friendly numerous microorganisms pro-
duce plant growth-promoting activities with specific action against coexisting
microorganisms toward the soil sustainability (Raaijmakers et al. 2009;
­Combes-­Meynet et al. 2011; Genilloud et al. 2011; Pineda et al. 2012; Meena et al.
2013; Maurya et al. 2014; Kumar et al. 2015; Verma et al. 2015b). Global agricul-
ture has to double food production by 2050 in order to feed the world’s growing
population and at the same time reduce its reliance on mineral/inorganic agricul-
16 Can Bacillus Species Enhance Nutrient Availability in Agricultural Soils? 369

tural inputs. To achieve this goal, there is an urgent need to harness the multiple
beneficial interactions that occur between soil microorganisms, plant, and the envi-
ronment. Beneficiary impacts of soil microorganisms enhance the sustainability of
soil–plant–environment ecosystem (Gupta 2012; Bahadur et al. 2016b; Das and
Pradhan 2016; Dominguez-Nuñez et al. 2016).

16.2 Soil Microbial Diversity

The beneficial influences of soil microorganisms on plant growth and development

include nitrogen fixing (Peix et al. 2001; Riggs et al. 2001; Marino et al. 2007),
phosphorus solubilization (Yasmin et al. 2004; Tajini et al. 2012; Verma et al. 2013),
potassium solubilization (Phua et al. 2012; Yadegari et al. 2012; Zhang et al. 2013:
Meena et al. 2014; Maurya et al. 2014; Saha et al. 2016a), zinc solubilization
(Mäder et al. 2010; Saravanan et al. 2007; Bahadur et al. 2016b), and indirect mech-
anisms such as productio n of phytohormones (Rashedul et al. 2009; Abbasi et al.
2011) such as auxins (Verma et al. 2013), siderophores (Filippi et al. 2011; Yu et al.
2011a, b), and PGPR from the rhizosphere to screen for their growth-­promoting
activity in plants under axenic conditions (Datta et al. 2011; Meena et al. 2015a,
2016; Singh et al. 2015; Verma et al. 2015a;).

16.2.1 Agricultural Important Soil Microorganisms

It has been reported that biological fertilization is an efficient method to supply

plants with their necessary nutrients. It is economically and eco-friendly recom-
mendable, because its results improved the agricultural and environmental sustain-
ability. During the past century, industrialization of agriculture has provoked a
significant and essential productivity increase, which has led to a greater amount of
food available to the general population. Along with this abundance, the appearance
of serious environmental and social problems came with the package: problems that
must be faced and solved in the not too distant future. Nowadays, it is urgent to
maintain that high productivity, but it is becoming urgent to alter as little as possible
the environment. Clearly we must then head for a more environmentally sustainable
agriculture while maintaining ecosystems and biodiversity. One potential way to
decrease negative environmental impact resulting from continued use of chemical
fertilizers, herbicides, and pesticides is the use of plant growth-promoting rhizobac-
teria (PGPR). This term was first defined by Kloepper and Schroth (1978) to
describe soil bacteria that colonize the rhizosphere of plants, growing in, on, or
around plant tissues that stimulate plant growth by several mechanisms. Since that
time, research activities aimed at understanding how these bacteria perform their
positive (or negative) effect have steadily increased, and many reports have been
published on these microorganisms. Although interactions between soil microor-
ganisms, plants–rhizosphere, and the environment have important consequences for
370 V.S. Meena et al.

ecosystem dynamics and changes in plant communities with time occur in concert
with changes in soil properties, the relationships between soil microbial community
and plant community dynamics are not fully understood (Van Der Putten 2003;
Saha et al. 2016b). Plants are able to modify the structure of microbial communities
in their rhizosphere (Berg and Smalla 2009), while soil microbes are important
regulators of plant productivity, both through direct effects and through regulation
of nutrient availability (Meena et al. 2014). However, the role of such interactions in
plant community dynamics with time has received little attention (Bartelt-Ryser
et al. 2005; Meena et al. 2015b, c).

16.2.2 The Bacillus Diversity in Agricultural Soils

Bacillus is the most abundant genus in the rhizosphere, and the PGPR activity of
some of these strains has been known for many years, resulting in a broad knowledge
of the mechanisms involved (Probanza et al. 2002; Mañero et al.2003). Naturally
present in the immediate vicinity of plant roots, B. subtilis is able to maintain stable
contact with higher plants and promote their growth (Dotaniya et al. 2016; Jaiswal
et al. 2016; Jha and Subramanian 2016). In a micro-propagated plant system, bacte-
rial inoculation at the beginning of the acclimatization phase can be observed from
the perspective of the establishment of the soil microbiota rhizosphere. B. lichenifor-
mis when inoculated on tomato and pepper shows considerable colonization and can
be used as a bio-fertilizer without altering normal management in greenhouses as
well as field condition (Bacon et al. 2001; Sessitsch et al. 2002; Wu et al. 2005).
B. megaterium is very consistent in improving different root parameters in mint.
Phosphorus-solubilizing bacteria (PSB) B. megaterium var. phosphaticum
(Lavakusha et al. 2014) and potassium-solubilizing bacteria (KSB) B. mucilaginosus
(Meena et al. 2014; Maurya et al. 2014) when inoculated in nutrient-­limited soil
showed that rock materials (P and K rocks) and both bacterial strains consistently
increased mineral availability, uptake, and plant growth of pepper and cucumber,
suggesting its potential use as bio-fertilizer (Han et al. 2006; Supanjani et al. 2006).
Soil is the main reservoir of the potential bacterial rhizosphere community (Berg
and Smalla 2009). Evidence is increasing that plants actively select specific ele-
ments of their bacterial rhizosphere micro-flora, establishing a habitat which is
favorable for the soil–plant–environment system (Robin et al. 2007; Houlden et al.
2008; Rudrappa et al. 2008). The soil–matrix is a favorable niche for bacteria since
both temperature and humidity are relatively sustainable (Ranjard et al. 2000;
Sessitsch et al. 2001), mineral composition (Carson et al. 2009), and agricultural
practices (Rooney and Clipson 2009; Saha et al. 2016b). The neutral soil reaction is
the most favorable condition for higher bacterial diversity, whereas acidic soils were
least diverse; it’s favorable for fungus growth and development. Bacterial popula-
tion revealed by culture-dependent techniques represents only 1–10 % of the total
bacterial micro-flora present in soil and is now known as the great plate count anom-
aly (Amann et al. 1995; Meena et al. 2015d, e).
16 Can Bacillus Species Enhance Nutrient Availability in Agricultural Soils? 371

16.2.3 Soil–Plant–Microbe System

Soil–plant–microbe interactions in the rhizosphere soils are responsible for various

processes that influence plant growth and development and nutrient mobilization
(Awasthi et al. 2011; Singh 2013); a wide range of beneficial microorganisms (e.g.,
bacteria, fungi, and actinomycetes) associated with plant roots have the ability to
promote the growth of the host plant under natural as well as agroecosystem by vari-
ous mechanisms, namely, fixation of atmospheric nitrogen (Glick et al. 2007), phos-
phorus (Verma et al. 2012a), potassium (Zhang et al. 2013), and zinc solubilization
(Bapiri et al. 2012), and production of plant growth regulators (Meena et al. 2012;
Miransari 2011; Rajkumar et al. 2012; Verma et al. 2012b). Besides, the plant-asso-
ciated microbes residing in the rhizosphere enhance the mobility and availability of
plant nutrients to the plants through release of chelating agents, acidification, and
redox changes (Glick et al. 2007; Rajkumar et al. 2012). It is also well known that
these microbes can utilize the plant-derived substances (e.g., root exudates) com-
prising different compounds (e.g., organic acids, sugars, vitamins, and amino acids)
as major nutrients for their growth and development (Berendsen et al. 2012; Dakora
and Phillips 2002; Ryan et al. 2001). On the other side, plants stimulate or inhibit
the growth of specific microorganisms through releasing secondary metabolites
(e.g., pyrones, sesquiterpenes) into the rhizosphere (Reino et al. 2008; Berendsen
et al. 2012; Chakraborty et al. 2012). An example of bacterial stimulation of maize
plant root shoot growth is shown in Fig. 16.1.

Crop & Soil

Imbalance use
management
Crop removal

of fertilizers
practices

Soil reaction Oxidation & Reduction

Adsorption & Desorption Mineralization & Immobilization

Water
Erosion
Leaching

Nutrients & Soil

physico-chemical
factors

Root Exudates Rhizospheric

& PGRs community

Fig. 16.1 Schematic illustration of how soil and crop management practice factors influence
nutrient availability under soil–plant system
 372 V.S. Meena et al.

16.3 Current Nutrient Status of Agricultural Soils

A recent review of worldwide data on N use efficiency for cereal crops from
researcher-managed experimental plots reported that single-year fertilizer N
recovery efficiencies are ~65 % for corn, ~57 % for wheat, and ~46 % for rice.
Differences in the scale of farming operations and management practices (i.e.,
tillage, seeding, weed and pest control, irrigation, harvesting) usually result in
lower nutrient use efficiency (Kumar et al. 2016; Masood and Bano 2016; Meena
et al. 2016). Nitrogen recovery in crops grown by farmers rarely exceeds ~50 %
and is often much lower. A review of best available information suggests average
N recovery efficiency for fields managed by farmers ranges from about 20 % to 30
% under rainfed conditions and 30 to 40 under irrigated conditions. Looked at N
fertilizer recovery under different cropping systems and reported 37 % recovery
for corn grown in the north central USA. They found N recovery averaged 31 %
for irrigated rice grown by Asian farmers and 40 % for rice under field-specific
management. In India, N recovery averaged 18 % for wheat grown under poor
weather conditions, but 49 % when grown under good weather conditions (von
Braun 2007; Rajkumar and Freitas 2008a, b; Khamna et al. 2010). Phosphorus (P)
efficiency is also of interest because it is one of the least available and least mobile
mineral nutrients. First year recovery of applied fertilizer P ranges from less than
10 % to as high as 30 % (Fig. 16.2).
However, because fertilizer P is considered immobile in the soil and reaction
(fixation and/or precipitation) with other soil minerals is relatively slow, long-
term recovery of P by subsequent crops can be much higher. There is little infor-
mation available about potassium (K) use efficiency. However, it is generally
considered to have higher use efficiency than N and P because it is immobile in
most soils and is not subject to the gaseous losses that N is or the fixation reac-
tions that affect P. First year recovery of applied K can range from 20 % to 60 %
(Fig. 16.3).

450
400
N+P+K (kg/ha)

350
300
250
200
150
100
50
0

Fig. 16.2 The worldwide nutrients (NPK) consumption in agricultural production system
16 Can Bacillus Species Enhance Nutrient Availability in Agricultural Soils? 373

16.5 15.00
14.5
12.5
10.5
8.5 7.50 7.00 6.50 6.00
6.5
4.5
2.5
0.5
1974-79 1992-97 1997-02 2002-07 2007-12

Fig. 16.3 Crop response to fertilizer (kg of food grain/kg NPK)

16.4 PGPR Mechanism of Bacillus Species

Bacillus species have the potential to act as a PGPR, nutrient solubilization, and
bioremediation, to enhance crop growth, yield, and nutrient uptake by different
mechanisms that contributed through direct and indirect mechanisms in the devel-
opment of sustainable soil–plant–environment systems (Schippers et al. 1995).
The generally plant growth-promoting bacteria function in three different ways –
synthesizing particular PGR compounds for the growth and development of plants
(Zahir et al. 2004), facilitating the mineralization or solubilization of mineral from
fixed form to plant available form or soil solution that can help to enhance the nutri-
ents’ uptake from the soil (Cakmakci et al. 2006), and helping to reduce the chances
of disease infection or preventing the agricultural crops from insect, pest, and dis-
eases (Raj 2004; Saravanakumar et al. 2008; Meena et al. 2015f; Prakash and Verma
et al. 2016; Priyadharsini and Muthukumar 2016).

16.4.1 Direct and Indirect Mechanisms

The mechanisms of PGPB-mediated enhancement of plant growth and yield of many

crops are not yet fully understood (Dey et al. 2004). However, possible explanations
include (a) the ability to produce a vital enzyme, 1–aminocyclopropane–1–carboxyl-
ate (ACC) deaminase, to reduce the level of ethylene in the root of developing plants
thereby increasing the root length and growth (Li et al. 2006; Meena et al. 2013;
Verma et al. 2013); (b) the ability to produce hormones like auxin, i.e., indole acetic
acid (IAA) (Patten and Glick 2002), abscisic acid (ABA) (Dangar and Basu 1987;
Dobbelaere et al. 2003), gibberellic acid (GA), and cytokinins (Dey et al. 2004); (c) a
symbiotic nitrogen fixation (Kennedy et al. 2004); (d) antagonism against phyto-
pathogenic bacteria by producing siderophores, ß-1,3-glucanase, chitinases, antibiotic,
fluorescent pigment, and cyanide (Cattelan et al. 1999; Pal et al. 2001; Glick and
374 V.S. Meena et al.

Indirect Mechanisms Direct Mechanisms

Phytohormones (Cytokine, GAs, IAA, Ethylene etc)
Lytic Enzyme Zn-solubilization

oting Activities
H2S Production rom of K-Solubilization
P B

th

ac
row
Strach hydrolysis

illu
P-Solubilization

tG

ss
Plan

pp
Siderophore Ammonia production

Antibiotic production
Sequestration of iron

Competitions
Cellulose degradation

Ethylene N-fixer

Induced systematic resistance Acid production (Organic & Inorganic)

Bioremediation

Fig. 16.4 Mechanism of plant growth-promoting Bacillus species. (a) Direct mechanism (e.g.,
N2-fixer, phosphorus, potassium and zinc solubilization, etc.). (b) Indirect mechanism (e.g., IAA,
GAs, cytokinins and certain VOCs, etc.), both mechanism enhance plant mineral uptake and pro-
ductivity of crop

Stearns 2011); (e) solubilization and mineralization of nutrients, particularly mineral

phosphates and potassium (Maurya et al. 2014; Lavakusha et al. 2014; Meena et al.
2014); (f) enhanced abiotic stress (Saleem et al. 2007; Stajner et al. 1997); and (g)
production of water-soluble B group vitamins such as niacin, pantothenic acid, thia-
mine, riboflavin, and biotin (Revillas et al. 2000; Zhuang et al. 2007; Raghavendra
et al. 2016; Rawat et al. 2016; Saha et al. 2016a) (Fig. 16.4).

16.4.2 Nitrogen Fixer

The mineralization of soil organic nitrogen (N) through nitrate to gaseous N2 by soil
microorganisms is a very important process in global N cycling. This cycle includes
N mineralization, nitrification, denitrification, and N2 fixation. A number of bacterial
species belonging to the genera Bacillus, Azospirillum, Alcaligenes, Arthrobacter,
Acinetobacter, Burkholderia, Enterobacter, Erwinia, Flavobacterium, Pseudomonas,
Rhizobium, and Serratia (Yu et al. 2012; Braghini Sa et al. 2012; Thepsukhon et al.
2013) are associated with the plant rhizosphere and are able to exert a beneficial
effect on plant growth and development. Nowadays new techniques have identified a
wide range of organisms with the plant rhizosphere with the capacity to carry out
biological nitrogen fixation (BNF) – greatly expanding our appreciation of the
16 Can Bacillus Species Enhance Nutrient Availability in Agricultural Soils? 375

diversity and ubiquity of N fixers – but our understanding of the rates and controls of
BNF at ecosystem and global scales has not advanced at the same pace. Nevertheless,
determining rates and controls of BNF is crucial to placing anthropogenic changes to
the N cycle in context and to understanding, predicting, and managing many aspects
of global environmental change. Here, we estimate terrestrial BNF for a preindustrial
world by combining information on N fluxes with 15 N relative abundance data for
terrestrial ecosystems. Our estimate is that preindustrial N fixation was 58 (range of
40–100) TgN fixed yr 21; adding conservative assumptions for geological N reduces
our best estimate to 44 TgNyr 21. This approach yields substantially lower estimates
than most recent calculations; it suggests that the magnitude of human alternation of
the N cycle is substantially larger than has been assumed (Saha et al. 2016b; Sharma
et al. 2016; Shrivastava et al. 2016).

16.4.3 Phosphorus Solubilizers

The role of phosphorus mobilizers and solubilizers is more important in soil–plant

system because only ~15 % of the phosphorus fertilizer is directly available to the plant
growth and development and the rest of the 85 % is lost by different processes like
runoff and P fixation due to unfavorable soil conditions. However, eminent soil fertility
scientists recognize that soil reactions with applied phosphate limit its direct uptake by
plants in the short term; the long-term recovery can approach 90 %, because phospho-
rus is retained in the soil in slowly available forms (Syers 2003; Panhwar et al. 2012).
Phosphate solubilization by rhizospheric microorganisms in mineral phosphate
solubilization was known as early as 1903. Since then, there have been extensive
studies on the mineral phosphate solubilization by naturally abundant rhizospheric
microorganisms (Fig. 16.5). Strains from bacterial genera Pseudomonas, Bacillus,
Rhizobium, and Enterobacter along with Penicillium and Aspergillus fungi are the
most powerful P solubilizers (Whitelaw 2000). B. megaterium, B. circulans, B.
­subtilis, B. polymyxa, and B. sircalmous could be referred as the most important
strains (Verma et al. 2013; Meena et al. 2014; Yu et al. 2012).

16.4.4 Potassium Solubilizers

K-solubilizing bacteria are able to release potassium from insoluble minerals

(Sugumaran and Janarthanam 2007; Basak and Biswas 2009, 2012; Kalaiselvi and
Anthoniraj 2009; Parmar and Sindhu 2013; Zarjani et al. 2013; Prajapati et al. 2013;
Zhang et al. 2013; Gundala et al. 2013; Archana et al. 2012, 2013; Sindhu et al.
2012). In addition, researchers have discovered that K-solubilizing bacteria can pro-
vide beneficial effects on plant growth through suppressing pathogens and improv-
ing soil nutrients and structure. For example, certain bacteria can weather silicate
minerals to release potassium, silicon, and aluminum and secrete bioactive
376 V.S. Meena et al.

Fig. 16.5 The plant growth-promoting activities of Bacillus species, like potassium-solubilizing
bacteria (KSB), phosphorus-solubilizing bacteria (PSB), iron-sequestering bacteria (siderophore-­
producing bacteria), cellulose-degrading activities, pectinase-producing bacteria, and
phytohormone-­producing bacteria (IAA, GA3, ethylene, etc.)

materials to enhance plant growth (Fig. 16.5). These bacteria are widely used in
biological K fertilizers and biological leaching (Lian et al. 2002; Bosecker 1997).
The considerable populations of potassium-solubilizing microorganisms are present
in rhizospheric soil which promotes the plant growth (Sperberg 1958).
It is generally accepted that the major mechanism of mineral K solubilization is
the action of organic acids synthesized by rhizospheric microorganism. Productions
of organic acids result in acidification of the microbial cell and its surroundings
environment which promote the solubilization of mineral K. Silicate bacteria were
found to resolve potassium, silicon, and aluminum from insoluble minerals. Silicate
bacteria exert beneficial effects upon plant growth and yield. The KSB can promote
K solubilization from silicate mineral and is very important to enhance the fertility
status of soils. Rhizospheric microorganisms contribute directly and indirectly to
the physical, chemical, and biological parameters of soil through their beneficial or
detrimental activities (Meena et al. 2015g, h; Sindhu et al. 2016; Teotia et al. 2016).

16.4.5 Zinc Solubilizers

Zinc is predominantly taken up as a divalent cation, Zn2+, but in some cases of cal-
careous and high pH, it is believed to be taken up as a monovalent cation ZnOH+.
Zinc interactions in both plants and soils are quite complex and play a major role in
16 Can Bacillus Species Enhance Nutrient Availability in Agricultural Soils? 377

how and when we should apply zinc to a crop. Increasing the Zn and Fe concentra-
tion of food crop plants, resulting in better crop production and improved human
health is an important global challenge. Among micronutrients, Zn deficiency is
occurring in both crops and humans (White and Zasoski 1999; Welch and Graham
2004). Zinc is required in relatively small concentrations in plant tissues (5–100 mg/
kg). Zn deficiency is well reported in the soils of much of the world. The deficiency
of Zn in cereals especially rice is nutritionally a major problem. Cereals play in
satisfying daily calorie intake in the developing world, but the Zn concentration in
the grain is inherently very low, particularly when grown on Zn-deficient soils.
The major reason for the widespread occurrence of zinc deficiency problems in crop
plant is the low solubility of Zn in soils rather than low total amount of Zn. Zinc-
solubilizing bacteria (ZSB) help to solubilize the fixed form of Zn and increase uptake
of Zn leading to fortification of grains with Zn (Bapiri et al. 2012). Soil microorganisms
require various nutrients for their growth and metabolism. Among the nutrients, zinc is
an element present in the enzyme system as cofactor and metal activator of many
enzymes (Parisi and Vallee 1969). This causes transformation of about 96–99 % of
applied available zinc to various unavailable forms (Fig. 16.5). The zinc thus made
unavailable can be reverted back to available form by inoculating a bacterial strain capa-
ble of solubilizing it. Since zinc is a limiting factor in crop production, importance of
ZSB has an immense in zinc nutrition to plants (Bapiri et al. 2012; Verma et al. 2013).

16.4.6 Fe Sequestration

Iron (Fe) deficiency is a worldwide problem that is directly correlated with poverty
and food insecurity. Approximately one third of the world’s population suffers from
Fe deficiency-induced anemia, 80 % of which are in developing countries (Boccio
and Iyengar 2003; Miethke and Marahiel 2007). Total Fe content in soil is relatively
high, but its availability to soil microorganisms is low in aerated soils because the
prevalent form (Fe3+) is poorly soluble. Plants and microorganisms have developed
mechanisms to increase Fe uptake (Marschner 1995; Rajkumar et al. 2010). In
plants, there are two different strategies in response to Fe deficiency. Strategy I
plants (dicots and non-graminaceous monocots) release organic acid anions which
chelate Fe. Iron solubility is also increased by decreasing the rhizosphere pH, and
Fe uptake is enhanced by an increased reducing capacity of the roots (Fe3+ → Fe2+).
Strategy II plants (Poaceae) release phytosiderophores that chelate Fe3+ (Von Wiren
et al. 1993; Sinha and Mukherjee 2008; Sullivan et al. 2012). Under Fe deficiency
stress, soil microorganisms release organic acid anions or siderophores that chelate
Fe3+. After movement of the ferrated chelate to the cell surface, Fe3+ is reduced
either outside or within the cell (Neilands 1984). Microorganisms produce a range
of siderophores, e.g., ferrichromes by fungi and enterobactin, pyoverdine, and fer-
rioxamines by bacteria (Von Wiren et al. 1993; Ma et al. 2011). Rhizobacterial
strain significantly influences Fe uptake by agricultural crop (Yu et al. 2011a, b;
Sadeghi et al. 2012; Socha and Guerinot 2014).
378 V.S. Meena et al.

Fe was supplied either as microbial siderophores (pseudobactin [PSB] or ferriox-

amine B [FOB]) or as phytosiderophores obtained as root exudates from barley
(epi-3-hydroxy-mugineic acid [HMA]) under varied population densities of rhizo-
sphere microorganisms (axenic, uninoculated, or inoculated with different microor-
ganism cultures). When maize was grown under axenic conditions and supplied
with FeHMA Socha and Guerinot 2014), Fe uptake rates were 100–300 times higher
compared to those in plants supplied with Fe siderophores (Fig. 16.5). Fe from both
sources was taken up without the involvement of an extracellular reduction process.
The supply of FeHMA enhanced both uptake rate and translocation rate to the shoot
(>60 % of the total uptake). However, increased density of microorganisms resulted
in a decrease in Fe uptake rate (up to 65 %), presumably due to microbial degrada-
tion of the FeHMA. In contrast, when FeFOB or FePSB was used as the Fe source,
increased population density of microorganisms enhanced Fe uptake. The enhance-
ment of Fe uptake resulted from the uptake of FeFOB and FePSB by microorgan-
isms adhering to the rhizoplane or living in the free space of cortical cells. The
microbial apoplastic Fe pool was not available for root to shoot transport or, thus,
for utilization by the plants (Socha and Guerinot 2014). These results, in addition to
the low uptake rate under axenic conditions, are in contrast to earlier hypotheses
suggesting the existence of a specific uptake system for Fe siderophores in higher
plants. The bacterial siderophores PSB and FOB were inefficient as Fe sources for
plants even when supplied by stem injection. It was concluded that microorganisms
are involved in degradation processes of microbial siderophores, as well as in com-
petition for Fe with higher plants (Crowley et al. 1992; Socha and Guerinot 2014).
Fe sequestration of B. megaterium in iron-deficient medium detected in the expo-
nential phase of growth seems not to be affected by the glucose availability and was
not related with the onset of endospore formation (Chincholkar et al. 2007). The car-
bon source affected the siderophore production by B. megaterium (Socha and Guerinot
2014). Among the carbon sources tested, the growth on glycerol promoted the highest
siderophore production. The increase of argentine concentration in the culture medium
did not enhance the siderophore production. The agitation had a positive effect on the
growing of B. megaterium and siderophore production. To our knowledge, this is the
first work that describes the physiological response of B. megaterium in terms of sid-
erophore production (Das et al. 2007; Socha and Guerinot 2014).

16.5 I mpact of Bacillus Species on Yield and Nutrient

Uptake

Nowadays rapidly increasing rate of human population with reducing land holding size
due to urbanizations, industrialization, and modernization, by all these increasing
presser how to we increasing our food grain production in compared to population with
soil–plant–environment sustainability (Ilippi et al. 2011; Sullivan et al. 2012). One pos-
sible way to use of beneficially agricultural important microorganisms, with judicious
application of mineral as well as chemical fertilizer for sustainable crop production. In
16 Can Bacillus Species Enhance Nutrient Availability in Agricultural Soils? 379

this context many research studies reported that Bacillus species and other rhizobacte-
rial strains inoculated to soil significantly enhanced crop growth, yield, and nutrient
uptake (Yasmeen et al. 2012b; Velázquez et al. 2016; Yadav et al. 2016).
Bacillus spp. are used as PGPR with plant growth-promoting traits like phos-
phate, potassium, and zinc solubilization; N2 fixation and phytohormone production
(Liu et al. 2006; Lavakusha et al. 2014; Meena et al. 2014; Maurya et al. 2014) are
also being used as bio-inoculants for crop production. The Bacillus species are
reported to increase the yield in wheat (de Freitas et al. 2007; Cakmakci et al. 2007),
maize (Pal et al. 2001), sugar beet (Cakmakci et al. 2006), and spinach (Cakmakci
et al. 2007). According to Verma et al. (2012a) observed increase in growth and yield
of beans by co-inoculating Bacillus strains with other rhizobacteria significantly
influenced on nodule formation in pulse crops (Lavakusha et al. 2014; Liu et al.
2006; Yadav et al. 2010) and are widely used as plant health-promoting rhizobacteria
by reducing diseases and producing antibiotic (Verma et al. 2013) (Table 16.1).

16.6 I mplications of Efficient Soil Microorganisms

in Sustainable Agriculture

The various ways in which efficient soil microorganisms have been used over the
past fifth decade to modern sustainable technology, human and animal health, food
processing, food safety and quality, genetic engineering, environmental protection,
agricultural biotechnology, and in more effective treatment of agricultural. However,
microbial technologies have been applied to various agricultural and environmental
problems with considerable success in recent years; they have not been widely
accepted by the scientific community as it is often hard to consistently reproduce
their beneficial effects. We can enhance soil–plant–environment sustainability
through the use of efficient soil microorganisms for sustainable agricultural produc-
tion (Godfray et al. 2010). As discussed above, agriculture should consider maxi-
mizing the coadaptation between soil–plant–microbes in an effort to promote soil
microbial diversity (Badri et al. 2008 ; Yasin et al. 2016; Zahedi 2016).
Which implications does decoupling the coadapted soil–plant–microbial rela-
tionship have on sustainable agriculture? The soil environment is likely the most
complex biological community. Efficient soil organisms are extremely diverse and
contribute to a wide range of ecosystem services that are essential to the sustainable
function of natural and managed ecosystems. The efficient soil organism commu-
nity can have direct and indirect impacts on land productivity. Direct impacts are
those where specific efficient soil microorganisms affect crop yield immediately
(Broeckling et al. 2008). Indirect effects include those provided by soil organisms
participating in carbon and nutrient cycles, soil structure modification, and food
web interactions that generate ecosystem services that ultimately affect productiv-
ity. Research opportunities and gaps related to methodological, experimental, and
conceptual approaches may be helpful to enhance sustainable agricultural produc-
tion system.
380 V.S. Meena et al.

Table 16.1 Impact of Bacillus species on growth, yield, nutrient uptake, and plant growth-­
promoting activities with different crop species
Crop species Bacillus species Impact References
Cicer arietinum B. firmus strain Cold stress Khan et al. (2007)
NARS1
B. megaterium Phytohormones Verma et al. (2012b)
Lolium B. pumilus C2A1 Bioremediation Ahmad et al. (2006)
multiflorum
Cucumis melo B. subtilis Y-IV Plant growth, root Zhao et al. (2011)
colonization
Triticum aestivum B. pumilus strain S2 Enhance growth, yield, Abbasi et al. (2011)
B. pumilus S6-05 nutrient uptake Upadhyay et al. (2009)
Atriplex B. pumilus ES4 Phyto-stabilization De-Bashan et al.
lentiformis (2008)
Glycine max B. subtilis CICC1016 Siderophore, P Wahyudi et al. (2011)
B. sphaericus NUC-5 solubilization,
B. cereus strain SS-07 antagonism with F.
oxysporum, S. rolfsii, R.
B. pumilus
solani
B. shandongensis SD
Oryza sativa B. pumilus strain S68 ACC producing, PGRs Lavakush et al. 2014
B. sp SB1-ACC3
Artemisia annua B. subtilis strain Nitrogen fixing Awasthi et al. (2011)
Daz26
Fragaria spp. B. subtilis NA-101 IAA equivalents, Pereira et al. (2011)
B. subtilis NA-120 siderophore, strawberry
root, and shoot growth
Solanum B. strain Phosphorus Calvo et al. (2010)
tuberosum solubilization, IAA
Zea mays B. sp. Seed germination and Ngoma et al. (2014)
root shoot growth
Prunus cerasus B. subtilis OSU – 142 Fruit set, pomological Karakurt et al. (2011)
cv. Kutahya B. megaterium M and chemical
characteristics, color
values
Piper nigrum B. subtilis CAS15 Siderophore producing Yu et al. (2011a)
Lycopersicon B. amyloliquefaciens Controlling bacterial Wei et al. (1996)
esculentum QL5 wilt
B. amyloliquefaciens
QL18
Juglans spp. B. megaterium Nitrogen fixating, PSB Yu et al. (2012)
Lycopersicon B. subtilis Antifungal, nutrient Nihorimbere et al.
esculentum availability (2010)
Mammillaria B. megaterium M1PCa Mobilization of Lopez et al. (2012)
fraileana elements from rocks, Puente et al. (2009a, b)
mineral degradation
(continued)
16 Can Bacillus Species Enhance Nutrient Availability in Agricultural Soils? 381

Table 16.1 (continued)

Crop species Bacillus species Impact References
Zea mays B. mojavensis Maize seedling growth Bahadur et al. (2016b)
and nutrient uptake
Bouteloua B. spp. Phytoremediation, Ma et al. (2011)
dactyloides PGPR
Zea mays B. spp. Drought tolerant Singh et al. (2013)
Brassica juncea B. spp. Ba32 PGRs, P solubilization Rajkumar et al. (2006)
Rajkumar et al.
(2008a, b)
Brassica juncea B. subtilis SJ-101 IAA, P solubilization, Zaidi et al. (2006)
increased shoot length, Rajkumar et al. (2008)
fresh and dry weights
Brassica napus B. subtilis RJ16 (RS) IAA, Cd-mobilization, Sheng and He (2006)
increased root Rajkumar et al. (2009)
elongation (gnotobiotic
conditions), shoot and
root dry weight (pot
experiment)
Sorghum bicolor B. subtilis Increase root shoot Abou-Shanab et al.
B. pumilus biomass (2008)
Lycopersicon B. amyloliquefaciens PGPR, P solubilization Nihorimbere et al.
esculentum S499 (2011)
Sorghum bicolor B. mucilaginosus Potassium solubilizing Basak and Biswas
var. sudanense (2010)
Glycine max B. subtilis Nutrient uptake, plant Bais et al. (2002)
growth
Pinus thunbergii B. cereus Growth, nutrient uptake Wu et al. (2011)
Actinidia B. subtilis OSU142, Rooting and root Erturk et al. (2010)
deliciosa B. megaterium RC01 growth
Musa paradisiaca B. amyloliquefaciens Fusarium wilt and plant Baset Mia et al. (2010)
W19 growth, increased
biomass
Brassica napus B. licheniformis Cr, Cu, Pb, and Zn Brunetti et al. (2011)
BLMB1 phytoextraction Rajkumar et al. (2010)
Triticum aestivum B. subtilis PGRs, nutrient uptake Upadhyay et al. (2011,
2012)
Zea mays B. megaterium Vegetative growth, Singh et al. (2013)
yield
Arabidopsis B. subtilis P solubilization, PGRs Zhang et al. (2008)
thaliana
Persea gratissima B. megaterium Phytohormones, Nadeem et al. (2012)
growth, yield
Raphanus sativus B. subtilis, Bioremediation, yield, Kaymak et al. (2009)
B. megaterium PGRs
Medicago sativa B. pumilus Growth, yield, nutrient Medina et al. (2003)
B. licheniformis uptake
(continued)
382 V.S. Meena et al.

Table 16.1 (continued)

Crop species Bacillus species Impact References
Lycopersicon B. megaterium PGRs, growth, yield Singh et al. (2013)
esculentum
Manihot B. megaterium Cav. P solubilization Chen et al. (2014)
esculenta Crantz cy3
Oryza sativa B. circulans P2 Increased rice grain Panhwar et al. (2012)
B. megaterium P5 yield
Spinacia oleracea B. megaterium RC07 PGRs, vegetative Çakmakçi et al. (2007)
B. subtilis RC11 growth, bioremediation
Sorghum bicolor B. polymyxa Increased grain and dry Alagawadi and Gaur
matter yields and N and (1992)
P uptake
Cicer arietinum B. megaterium Increased dry matter, Verma et al. (2013)
grain yield and P
uptake, nodulation, N
fixation
Helianthus B. megaterium M-13 Increased yield, oil, Ekin (2010)
annuus protein content
Solanum B. polymyxa Increased yield, P Kundu and Gaur
tuberosum uptake (1980)
Rubus idaeus B. megaterium Increased crop yield Orhan et al. (2006)
Ammi visnaga B. simplex Increased root, shoot Hassen et al. (2010)
B. cereus length, dry weight
Fragaria B. megaterium Increased fruit yield, Esitken et al. (2010)
ananassa nutrient contents
Curcuma longa B. megaterium Plant growth and yield Sumathi et al. (2011)
Momordica B. subtilis Enhanced yield, quality, Kumar et al. (2012a)
charantia root length, and dry
root weight
Phyllanthus B. coagulans Improved growth, yield Earanna (2001)
amarus
Begonia B. coagulans Biomass yield, Selvaraj et al. (2008)
malabarica nutrients, and
secondary metabolites
Mentha piperita B. megaterium Root length, dry matter Kaymak et al. (2008)
Solanum viarum B. coagulans P, Fe, Zn, Cu, and Mn Hemashenpagam and
content, secondary Selvaraj (2011)
metabolites
Sphaeranthus B. subtilis Enhanced growth, Sumithra and Selvaraj
amaranthoides biomass, nutrition (2011)
Withania B. circulanse Increased plant height, Rajasekar and Elango
somnifera root length, and (2011)
alkaloid content
Rosmarinus B. megaterium Increased oil content, Abdullah et al. (2012)
officinalis B. circulanse yield in fresh herb, and
total CHO
16 Can Bacillus Species Enhance Nutrient Availability in Agricultural Soils? 383

16.7 Future Prospect

The Bacillus species are a major integral component of soil microbial community
and play an important role in the N fixation and phosphorus, potassium, zinc, and
iron cycles in soil–plant rendering the plants available forms of nutrients. These
bacterial strains have enormous potential for making use of fixed form of minerals
and very slowly available nutrients under soil–plant systems with low availability in
tropical and subtropical countries. The mechanism of mineral solubilization by
Bacillus species has been studied in detail, but the K and Zn solubilization and Fe
sequestration are a complex phenomenon affected by many factors, such as poten-
tial of bacterial strain used, nutritional status of soil, mineral type, amount of min-
eral, size of mineral particles, and environmental factors. Moreover, the sustainability
of the Bacillus species after inoculation in soil as well as seed and seedling treat-
ment is also important for mineral availability to benefit sustainable crop growth
and development. Therefore, further study is needed to understand the problem of
development of efficient and indigenous Bacillus species with microbial consortium
for growth and yield of crops. Another big problem is the commercial propagation
of soil microorganism’s consortium and their preservation and transportation at
farmer’s fields for sustainable agricultural production.

16.8 Concluding Remarks

Climate change problems have raised great interest in eco-friendly sustainable agri-
cultural management practices. The use of growth-promoting rhizobacteria is a prom-
ising solution for sustainable soil–plant–microbes, environmentally friendly
agricultural production system. The studies on Bacillus species as plant growth-­
promoting activities in sustainable agriculture included isolating and screening antag-
onists targeting different diseases, evaluating their effectiveness in greenhouse as well
as field, dissecting their mechanisms, and enhancing nutrient availability in agricul-
tural soils. Research on improvement of Bacillus species through genetic engineering
is also conducted in order to increase effectiveness under unfavorable conditions.
Bacillus species control the damage to plants from phytopathogens and promote the
plant growth by a number of different mechanisms and enhance the availability of
nutrients for sustainable growth and development of agricultural production system.

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