Journal of Applied Microbiology ISSN 1364-5072

REVIEW ARTICLE

Bacillus species in soil as a natural resource for plant health

and nutrition
A.K. Saxena1, M. Kumar1, H. Chakdar1, N. Anuroopa2,3 and D.J. Bagyaraj2
1 ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, Uttar Pradesh, India
2 Centre for Natural Biological Resources and Community Development, Bangalore, Karnataka, India
3 Government Science College, Nrupathunga Road, Bangalore, Karnataka, India

Keywords
Bacillus, biocontrol, PGPR, plant nutrition,
plant protection.
Correspondence
D. Joseph Bagyaraj, INSA Honorary Scientist &
Chairman, CNBRCD, 41 RBI Colony, Anand
Nagar, Bangalore 560024, India.
E-mail: djbagyaraj@gmail.com
2019/1228: received 22 August 2019, revised
19 October 2019 and accepted 29 October
2019
doi:10.1111/jam.14506
Abstract
The genus Bacillus is one of the predominant bacterial genera found in soil,
and several species of this genus have been reported from diverse ecological
niches. Endowed with tremendous genetic and metabolic diversity, Bacillus
spp. serve multiple ecological functions in soil ecosystem from nutrient cycling
to conferring stress tolerance to plants. Members of the genus Bacillus are
known to have multiple beneficial traits which help the plants directly or
indirectly through acquisition of nutrients, overall improvement in growth by
production of phytohormones, protection from pathogens and other abiotic
stressors. This functionally versatile genus is one of the most commercially
exploited bacteria in the agro-biotechnology industry. Still its potential has not
been realized sufficiently and requires an emphasis towards translating the
relevant technologies from laboratory to land for the benefit of mankind.

Introduction Bacillus and nitrogen fixation

Microbial component of soil plays a critical role in keeping
soil alive and functional, exercising several indispensable func-
tions like soil formation, decomposition of dead and decayed
organic matter, cycling of macro and micronutrients and
removal/transformation of toxic chemicals into non-toxic
forms (Van Elsas et al. 2006). Free-living beneficial bacteria
imparting health benefits to crop plants are collectively called
as plant growth-promoting rhizobacteria (PGPR) comprising
of different genera like Azospirillum, Pseudomonas, Azotobac-
ter, Klebsiella, Enterobacter, Alcaligens, Arthrobacter,
Burkholderia, Bacillus and several others (Bashan et al. 2014).
Several species of the genus Bacillus like B. megaterium, B. cir-
culans, B. coagulans, B. subtilis, B. azotofixans, B. macerans, B.
velezensis, etc. are reported as PGPR (Goswami et al. 2016;
Fan et al. 2018). The various direct and indirect mechanisms
of plant growth promotion by Bacillus spp. are nitrogen fixa-
tion, solubilization and mineralization of phosphorus and
other nutrients, phytohormone production, production of
siderophores, antimicrobial compounds and hydrolytic
enzymes, induced systemic resistance (ISR) and tolerance to
abiotic stresses (Goswami et al. 2016) (Fig. 1a,b).
The ability to fix atmospheric nitrogen rests with the
domain Eubacteria and Archaea. Diverse species of Bacil-
lus comprising B. cereus, B. circulans, B. firmus, B. pumi-
lus, B. licheniformis, B. megaterium, B. subterraneous, B.
aquimaris, B. vietnamensis and B. aerophilus are known to
fix atmospheric nitrogen (Ding et al. 2015; Yousuf et al.
2017). Diazotrophic B. pumilus, B. altitudinis and B.
safensis were isolated from rhizosphere of maize, rice and
crabgrass respectively (Habibi et al. 2014). A total of 27
different diazotrophic Bacillus spp. were isolated from
sunflower rhizosphere of which two strains recorded acet-
ylene reduction assay (ARA) values above 10 nmol C2H4
mg protein h 1 (Ambrosini et al. 2016). A novel dia-
zotrophic bacterium Bacillus rhizosphaerae was isolated
from sugarcane rhizosphere and could increase dry bio-
mass of plants (Madhaiyan et al. 2011). To ensure the
nitrogen fixation capability and diversity analysis of dia-
zotrophs, the most widely used gene marker is nifH
(Yousuf et al. 2017). A study on nitrogen fixing potential
of diverse species of Bacillus has reported the presence of
nifH gene and hence the capability to fix atmospheric

Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology 1583
Bacillus sp. in soil and plant health A.K. Saxena et al.

(a) (b)
Zn sol
Toxins
K
so
l
sol
P
Controls pest
infestation Controls
pathogen attack Ab
Enz. VoC
Siderophore

Antagonism

Alleviates
abiotic stress

HCN

Lytic
ISR/IST enzymes IAA
Lytic
Or enzymes
ga
nic
ac
ids
Solu
Phyto- due blizati
to p o
hormones Hd n
rop
Fe Fe chelating
Soluble Fixed insoluble
siderophore nutrient nutrient

Figure 1 (a) Overview of different plant beneficial mechanisms exerted by Bacillus spp. (b) Different plant growth-promoting traits exerted by
Bacillus spp. [Colour figure can be viewed at wileyonlinelibrary.com]

nitrogen in B. aerophilus, B. cereus, B. megaterium, B.
oceanisediminis, B. safensis, B. circulans and B. flexus. In
one of the study, out of 19 different Bacillus strains tested,
16 were positive for nifH gene (Yousuf et al. 2017). Bacil-
lus megaterium, B. marisflavi and B. cereus isolated from
rhizosphere of different field crops in China were found
positive for nifH gene. Experiment on nitrogenase activity
through ARA resulted positive only for B. megaterium
while B. marisflavi and B. cereus did not show any ARA
activity (Ding et al. 2005). In contrast to this, B. cereus
was found to show the highest nitrogenase activity among
42 different strains of Bacillus spp. studied by Ambrosini
et al. (2016). Bacillus aryabhattai, B. megaterium and B.
subtilis have been isolated as endophytic nitrogen fixers
from a Korean rice cultivar (Ji et al. 2014).
Bacillus and phosphorus nutrition
Phosphorus is the second most important nutrient after
nitrogen that limits the growth and yield of crop plants.
Plants can take up phosphorus in the form of HPO42
and H2PO4 (Saeid et al. 2018) but much of the phos-
phorus present in soil is unavailable to plants. Many soil
micro-organisms are endowed with the ability to solubi-
lize unavailable form of phosphorus to available form
and/or to mineralize organic phosphorus to available
form of phosphorus (Bhattacharyya and Jha 2012) and
are collectively called as phosphorus solubilizing micro-
organisms (PSMs). Many species of Bacillus like B. circu-
lans, B. cereus, B. fusiformis, B. pumilus, B. megaterium, B.
mycoides, B. coagulans, B. chitinolyticus, B. subtilis, etc.
have been reported as phosphorus solubilizers (Sharma
et al. 2013). A stress-tolerant isolate CB8A identified as B.
subtilis was reported to solubilize 806 mg l 1 of phos-
phate with gluconic acid and citric acid detected as major
organic acids. The strain is special in its ability to solubi-
lize P at wide range of temperature and pH (Mehta et al.
2013). Three species of Bacillus viz., B. megaterium, B.
subtilis and B. cereus were tested for solubilization of
phosphorus in the substrates like poultry bones, fish
bones and ash. All the three species produced organic
acids and there was a strong correlation between total
concentration of organic acids produced and the amount
of available phosphorus released from the substrates
(Saeid et al. 2018). As opposed to soils with high pH
where P is fixed as calcium phosphate, in acidic soils P is
often complexed with aluminium and iron. Thus in acid
soils, the PSMs have to solubilize P from the complexes
of aluminium and iron (Pradhan et al. 2018). Bacillus
megaterium M510 isolated from maize rhizosphere in the
eastern Himalayan region was found to solubilize both
aluminium phosphate and iron phosphate in addition to
moderate the solubilization of tricalcium phosphate
(Panda et al. 2016). This strain can be an effective PSM

1584 Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology
A.K. Saxena et al.
in both acidic and alkaline soils. Different forms of
organic phosphorus can collectively contribute to 30%–
50% of the total P in soil. Hence P mineralization can be
an effective means of P management in crop plants.
Phosphatases and phytases are two groups of enzymes
that catalyse conversion of organic phosphates to inor-
ganic phosphates. Bacillus flexus and B. megaterium are
shown to exhibit acid and alkaline phosphatase activity
(Ibarra-Galeana et al. 2017). Phytases are known to be
produced by B. subtilis, B. licheniformis and B. laevolacti-
cus (Farhat et al. 2008). In another study, B. cereus and
B. megaterium have been reported as organic phosphorus
mineralizing bacteria (Guang-Can et al. 2008).
Bacillus and phytohormone production
Auxins, gibberellins, cytokinins, ethylene (ET) and abscisic
acid are the well-known phytohormones produced by the
PGPR in soil. IAA production is reported in different spe-
cies of Bacillus like B. velezensis, B. subtilis, B. megaterium
and B. licheniformis (Lim and Kim 2009). An IAA-produc-
ing Bacillus sp. JH2-2 isolated from metal contaminating
site was found to promote growth of Indian mustard
under chromium stress, suggesting the role of this strain
in phytoremediation of chromium contaminated site
(Shim et al. 2015). Gibberellins are reported to be pro-
duced by B. pumilus, B. licheniformis, B. cereus, B. macro-
ides, B. velezensis and B. subtilis (Radhakrishnan and Lee
2016). Bacillus aryabhattai strain SRB02, isolated from soy-
bean rhizosphere, was found to produce high levels of
IAA, gibberellins and jasmonic acid (JA) and are found to
promote the growth of soybean and alleviate oxidative
stress (Park et al. 2017). Foliar spray with B. velezensis KE2
with the ability to produce gibberellins and IAA triggered
plant growth promotion and defence in sesame plants
(Radhakrishnan and Lee 2016). Bacillus subtilis, B. mega-
terium, B. licheniformis and B. velezensis have been demon-
strated for cytokinin production (Alina et al. 2015; Asari
et al. 2017). Bacillus velezensis UCMB5113, a strain-pro-
ducing cytokinin and IAA, is reported to stimulate the
growth of Arabidopsis thaliana through lateral root elonga-
tion and root hair formation (Asari et al. 2017). ET is an
important plant growth modulator and at higher levels
can lead to growth inhibition or even senescence. Many
PGPR are known to produce 1-aminocyclopropane-1-car-
boxylate (ACC) deaminase, an enzyme that cleaves ACC
and reduce the levels of ET (Glick, 2014). A multifunc-
tional PGPR, B. licheniformis K11, was shown to produce
ACC deaminase and provide tolerance to drought in pep-
per plants (Lim and Kim 2013). ACC deaminase activity
has been reported in various other species of Bacillus like
B. subtilis, B. firmus, B. circulans and B. globisporus (Xu
et al. 2014).
Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology
Bacillus sp. in soil and plant health
Bacillus and siderophore production
Siderophores are low-molecular weight metal chelating
compounds of the type hydroxamate and catecholate.
Siderophore-producing microbes can also inhibit the
growth of pathogens in the rhizosphere thereby confer-
ring biocontrol activity. With all these functions sidero-
phore-producing microbes help plant growth through the
mechanisms of increased iron uptake, heavy metal reme-
diation and biocontrol activity (Goswami et al. 2016).
Among the different species of Bacillus, siderophores are
known to be produced by B. anthracis, B. thuringiensis, B.
cereus, B. velezensis, B. atrophaeus, B. mojavensis, B.
licheniformis, B. pumilus, B. halodenitrificans and B. sub-
tilis (Ramadoss et al. 2013; Goswami et al. 2014). Inocu-
lating Alnus firma, a hyperaccumulator of metal ions,
with the siderophore producer B. thuringiensis GDB1
(also capable of producing ACC deaminase and solubiliz-
ing phosphorus) improved the efficiency of phytoremedi-
ation of heavy metal-contaminated site by this plant
(Babu et al. 2013). Yuan et al. (2014) have isolated B.
velezensis SQR-7, SQR-101 and SQR-29 which can pro-
duce both siderophores and IAA. These strains were
shown to protect tobacco plants from infection by the
bacterial pathogen Ralstonia solanacearum. Although the
major role of siderophore-producing bacteria is to help
plants in acquisition of iron, most of the studies con-
ducted to date have shown siderophore-producing Bacil-
lus spp. as biocontrol agents. The possible explanation for
this could be the iron-chelating Bacillus spp. in the rhizo-
sphere-outcompete pathogens which cannot produce such
metal chelators.
Role of Bacillus in potassium and other nutrients
uptake
Potassium is the third most important plant nutrient
after nitrogen and phosphorus which plays a major role
in plant growth and development. Its reserve in soil is
large, yet more than 98% of them are in plant non-avail-
able form. Potassium-solubilizing bacteria (KSB) can
make this unavailable form of potassium into available
form through the production of organic acids. Another
well-known mechanism for solubilization of K is the pro-
duction of extracellular polysaccharides which can dis-
solve potassium-bearing minerals and release potassium
into soil solution (Singh et al. 2015). Potassium solubi-
lization has been reported in various species of Bacillus
like B. velezensis, B. cereus, B. circulans, B. coagulans, B.
edaphicus, B. megaterium, B. subtilis, B. firmus, B.
mycoides, B. decolorationis and B. horikoshii (Verma et al.
2015). KSB when co-inoculated with N-fixers and P-solu-
bilizers can enhance the effect of N-fixers and P-
1585
Bacillus sp. in soil and plant health
solubilizers (Basak and Biswas 2010). Bacillus licheniformis
BHU18 was shown to solubilize potassium and produce
IAA. The strain was found to tolerate various regimes of
pH and hence can be an effective bioinoculant in both
acidic and alkaline soils (Saha et al. 2016). KSB are often
applied with a mineral form of potash like mica waste.
Recently B. pseudomycoides, a KSB, was isolated from tea-
growing soils of North east India and was found to
increase the availability of potassium in soil and uptake
in tea plants when inoculated with Mica waste (Pramanik
et al. 2019). Another important nutrient where Bacillus
can be found to play a major role is zinc. Zinc-solubiliz-
ing bacteria (ZSB) are known to produce various kinds
of organic and inorganic acids and chelating compounds,
through which complex unavailable forms of zinc are
made available to plants (Kumawat et al. 2017). Well-
known zinc solubilizers in the genus Bacillus are B. aryab-
hattai, B. subtilis, B. thuringiensis and B. tequilensis (Sha-
keel et al. 2015; Singh et al. 2017). The role of Bacillus in
iron has already been discussed in the siderophore section
of this review. Bacteria positively influencing nutrition of
plants in zinc and iron nutrition have got a major role to
play in microbe-mediated biofortification. ZSB B. aryab-
hattai was reported to biofortify wheat and soybean with
zinc (Ramesh et al. 2014). ZSB B. subtilis DS-178 inocula-
tion to wheat genotypes enhanced the uptake of Zn in
wheat grains by twofold as compared to uninoculated
control (Singh et al. 2017). A PGPR B. subtilis GB03 was
found to augment iron content in both Arabidopsis and
Cassava (Freitas et al. 2015).
Bacillus and plant growth promotion in crop
plants
The use of Bacillus as PGPR has been reported in many
different field and horticultural crops (Saxena et al.
2017). Two multifaceted PGPR strains Bacillus sp. and B.
cereus with ability to solubilize P, K and Zn and activities
against Pyricularia oryzae and Fusarium oryzae have
shown increased yield and zinc translocation towards
grains in basmati rice varieties (Shakeel et al. 2015). An
IAA-producing PGPR strain, B. altitudinis FD48, when
inoculated to rice was shown to modify root architecture
by regulating auxin-responsive genes (Ambreetha et al.
2018). Bacillus megaterium and B. safensis were reported
to enhance plant growth parameters like root and shoot
dry weight and seed weight under field condition in
wheat (Mukhtar et al. 2017). Auxin-producing strains, B.
velezensis S-134, B. muralis D-5, B. thuringiensis S-26 and
B. simplex D-1 capable of producing IAA, indole-3-car-
boxylic acid and indole-3-lactic acid were shown to alle-
viate the drought stress in wheat (Raheem et al. 2018). A
commercial microbial effector, B. velezensis FZB42 from
1586 Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology
A.K. Saxena et al.
Germany, when inoculated in maize plants along with the
application of compost significantly influenced the
growth and nutrient uptake. Enhanced photosynthetic
activity is also reported as shown by increase in gamma-
aminobutyric acid metabolites, glucose, fructose and ala-
nine in leaves of inoculated plants (Vinci et al. 2018). A
P-solubilizer B. megaterium mj1212 was shown to
increase the plant growth, contents of chlorophyll,
sucrose, glucose, fructose and amino acids in leaves indi-
cating enhanced photosynthetic activity in mustard (Kang
et al. 2014). A PGPR B. licheniformis A2 isolated from
rhizosphere of halotolerant plant Suaeda fruticosa from
Rann of Kutch was shown to increase the plant growth
of peanut both in the presence and absence of salt stress
(Goswami et al. 2014). Mineral (P and Zn)-solubilizing
bacteria Bacillus sp. AZ17 and Pseudomonas sp. AZ5 were
reported to improve nodule weight and number, straw
and grain yield and uptake of P and Zn in chickpea
plants under field conditions in a rainfed area (Zaheer
et al. 2019). Bacillus circulans CB7 isolated from apple
rhizosphere soil with multifaceted PGP traits like P-solu-
bilization, production of auxins, ACC deaminase and
siderophore was shown to have positive influence on the
plant growth parameters in tomato under net house con-
dition (Mehta et al. 2015). Bacillus subtilis with the ability
to produce IAA was shown to influence the plant growth


and yield of onion (Colo et al. 2014). Bacillus velezensis
FZB42, a model for plant growth promoting, and biocon-
trol strains of Bacillus have been shown to promote
growth and suppress diseases in various crops like potato,
cotton, wheat, tomato, strawberry and lettuce (Fan et al.
2018). The role of Bacillus as PGPR has also been
reported in various other crops like cotton, pepper, soy-
bean, green gram and sunflower (Passari et al. 2018;
Zahir et al. 2018). A list of few PGPR formulations based
on Bacillus spp. is given in Table 1.
Bacillus as biocontrol agent
The genus Bacillus is one of the most exploited microbial
groups for biological control of pathogens and pests. Bacil-
lus spp. are known to produce a great variety of metabo-
lites which can inhibit the growth and functions of cellular
organisms like bacteria, fungi, insects, nematodes and acel-
lular organisms like viruses. Genomes of Bacillus species
are packed with codes for machineries involved in biosyn-
thesis of secondary metabolites showing antimicrobial
properties, lytic enzymes, volatile organic compounds and
toxins. Bacillus can directly inhibit the growth of pests and
pathogens through the production of antimicrobial com-
pounds, enzymes or toxins while indirectly, the plant
immune response may be triggered through specific bacte-
rial elicitors. Bacillus-derived antimicrobial compounds
A.K. Saxena et al. Bacillus sp. in soil and plant health

Table 1 Bacillus based commercial formulations in different countries

Commercial formulations
Mechanisms of growth
Bacillus spp. promotion/crop protection References Product Country

B. velezensis Nutrient mineralization, auxin production, Asari et al. (2017) Hatake Japan
production of NRPs
B. velezensis Production of NRPs, Lytic enzymes, ISR Borris et al. (2019) RhizoVitalâ 42 (FZB42) Germany
B. velezensis ISR Berini et al. (2018) Amyprotec-42 (FZB42) Switzerland
B. megaterium var. P solubilization Panda et al. (2016) Symbion-Pâ India
phosphaticum
B. subtilis Zn and P solubilization Saeid et al. (2018) Green dual India
B. subtilis Production of Iturin Fira et al. (2018) Companion (GB03) USA
B. subtilis Deactivate heavy metal https://kiwabiotech.com. Jingaiguibao China
Accessed 17-10-2019
B. thuringiensis var. Cry 1 and Cry 2 toxins production Crickmore et al. (2015) Lepinox Plus (EG 2348) Italy
kurstaki
B. megaterium var. P solubilization Sharma et al. (2013) Fosfix Lithuania
phosphaticum
B. subtilis Antibiotic production Fira et al. (2018) Serenade (QST-713) USA

Strain numbers are given in parenthesis () in the ‘Product’ column.

and toxins are of special importance due to their possible
commercial exploitation. The major means of biological
control of pests and pathogens by Bacillus are discussed
below under different subheadings.
Antimicrobial metabolites
Members of the genus Bacillus like B. subtilis, B.
thuringiensis, B. cereus, B. velezensis, B. licheniformis etc.
are well known for their ability to produce antimicrobial
compounds. Stein (2005) reported that B. subtilis can
devote up to 5% of its genome towards the biosynthesis
of antimicrobial compounds and almost 10% of the gen-
ome of B. velezensis FZB42 is for synthesis of different
antimicrobial compounds (Borris et al. 2019). Majority of
the antimicrobial metabolites are the products of sec-
ondary metabolism and are generally short peptides.
Ribosomal peptides comprise mainly of bacteriocins
which act specifically against related bacteria through
interaction with the cell envelope. Subtilisin produced by
B. subtilis, haloduracin produced by B. halodurans and
lichenidin produced by B. licheniformis are some of the
examples of important Class I bacteriocins. Thuricin and
bacthuricin produced by B. thuringiensis, cerein produced
by B. cereus, etc. belong to Class II bacteriocin. Class III
bacteriocins are large protein with phospholipase activi-
ties. According to Zhao and Kuipers (2016), genes for
ribosomally synthesized peptides are highly abundant in
the genomes of B. thuringiensis, B. subtilis, B. cereus, B.
anthracis and B. velezensis.
Non-ribosomal peptides (NRPs) are synthesized
through ribosome independent enzyme-mediated
condensation of amino acid residues. More than 300 dif-
ferent precursor molecules can contribute in the assem-
blage of NRPs. The NRPs assembled by multi-domain
enzymes usually have fatty acid chains known as lipopep-
tides. Figure 2 presents the structure and family-wise dis-
tribution of NRPs present in Norine database (Flissi et al.
2016) and indicates that cyclic lipopeptides are one of the
most abundant NRPs in Bacillus. Among the members of
Bacillus, the genomes of B. subtilis, B. thuringiensis, B.
velezensis and B. cereus present high abundance of NRP
gene clusters (Zhao and Kuipers 2016). Among the
lipopeptides, iturin and surfactin are the most abundant
in Bacillus (Fig. 2). Surfactins are produced by a number
of Bacillus spp. with B. subtilis, B. licheniformis being
most predominant. Generally, surfactins contain a cyclic
heptapeptide forming a lactone bridge with b-hydroxy
fatty acids. Surfactins are one of the most powerful sur-
factants of biological origin and contribute to the swarm-
ing motility and biofilm-forming ability of Bacillus. These
cyclic heptapeptides are active against a number of bacte-
rial and fungal diseases like blast, stem rot, root rot, leaf
spot, soft rot etc. (Falardeau et al. 2013; Li et al. 2014;
Mora et al. 2015). Iturins are also heptapeptides contain-
ing b-amino fatty acids and are reported to be strong
antifungal peptides. Iturins, unlike surfactins, damage the
cells through the formation of ion-conducting pores (Fira
et al. 2018). These lipopeptides show strong activity
against fungal pathogens like Penicillium, Pestalotia, Gloe-
sporidium, Colletotrichum, Alternaria, Botrytis etc. (Falar-
deau et al. 2013; Ambrico and Truppo 2017).
Lipopeptides of Fengycin group can also damage the cells
through membrane destabilization and are reported to

Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology 1587
Bacillus sp. in soil and plant health A.K. Saxena et al.

show activities against pathogens like Fusarium, Rhizocto-

nia, Monilinia, etc. (Yanez-Mendizabal et al. 2012; Falar- 9% 1%
(a) 12%
deau et al. 2013; Guo et al. 2014).

Crystal proteins
Crystal (Cry) proteins, also known as d-endotoxins are 22%
produced specifically by B. thuringiensis (Bt). Cry toxins
represent the largest group of insecticidal proteins pro-
duced by Bacillus. According to the Bt toxin nomencla-
ture committee, till date 78 different Cry toxins with
Cry1 as the most predominant have been reported
(Crickmore et al. 2015). Diverse Cry toxins are produced
5%
by a wide variety of subspecies of B. thuringiensis. Differ-
ent strains of B. thuringiensis var kurstaki alone produce 51%
31 different types of Cry proteins with Cry1Aa and
Cry1Ac being the dominant. Cry4, Cry10 and Cry11 tox-
ins are predominantly produced by B. thuringiensis israe-
lensis. Cry1 toxins are mainly toxic to Dipteran, 1%
Lepidopteran and Coleopteran insects while Cry2 group 1%
is active against Dipteran, Lepidopteran and Hemipteran (b) 3% 3%
insects. Despite having wide array of Cry proteins, only 5%
Cry1 has been mostly exploited commercially. A number
of commercial products of Bt bioinsecticides (e.g. Dipel, 5% 1%
Thuricide, Biobit, Gnatrol, VectoBac, etc.) are available in
27% 2%
the market. The research on Bt-based biopesticides has
been taken to another level through application of nan-
otechnology. Nanotized Bt have been reported with
higher efficacy. Murthy et al. (2014) generated powders
14%
of Bt containing 32 to c.1100 nm-sized particles which
showed faster and higher mortality. Vineela et al.(2017)
synthesized Bt particles of 105–210 nm which showed
insecticidal activity similar to chemical insecticide Pro- 1%
fenophos against Spodoptera litura. Apart from nanotiza-
tion of Bt powders, the Cry toxins can be loaded onto
12%
nanomaterials. Cry1Ac protein has been loaded to mag-
nesium hydroxide nanoparticles which showed the 23%
enhanced adhesion on leaf surface of cotton and
increased mortality of Helicoverpa armigera (Rao et al. 1% 1%
2018). Not only biopesticides, Bt is also the most explored
Figure 2 Graphical representation of distribution of Bacillus-derived
and studied bacterial system in the field of plant biotech-
NRPs mined from Norine database (Flissi et al. 2016). (a) Distribution
nology for developing insect-resistant crop plants. A num- based on structure , Linear peptides; , Partial cyclic peptides; ,
ber of crops like maize, cotton, potato etc. have been Partial cyclic lipopeptides; , Cyclic peptides; , Cyclic lipopeptides;
genetically engineered to show resistance against a number , Other peptides; (b) distribution based on family. , BT Antibiotic;
of insects. For example, Monsanto Co. developed trans- , Bacilysin; , Edeine; , Gramicidin; , Kurstakin; , Bacillibactin;
genic cotton BollGard bearing Cry2Ab gene and conferring , Fengycin; , Polymyxin; , Bacitracin; , Cereulide; , Gratisin;
resistance against cotton bollworm, tobacco bollworm and , Iturin; , Mycobacillin; , Surfactin; , Tyrocidine. [Colour figure
can be viewed at wileyonlinelibrary.com]
pink bollworm while Mycogen Seeds developed Herculex
transgenic maize bearing Cry1F-encoding gene showing
resistance against European corn borer, Corn ear worm secreted out of the cell. These types of toxins can broadly
and Fall army worm (Roh et al. 2007). be divided into following two classes: (i) Vip (Vegetative
Apart from Cry toxins, during vegetative growth, few insectide protein) and (ii) Sip (Secreted insecticide pro-
strains of Bt can produce certain toxins which can be tein). Bt subspecies laterosporus, tolworthi, aizawai, etc.

1588 Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology
A.K. Saxena et al.
have been reported to produce Vip toxins. Vip1 and
Vip2 toxins constitute a binary toxin with high activity
against Coleopteran and Hemipteran insects while Vip3
toxins show activity against a range of Lepidopteran
insects (Palma et al. 2014). The Sip toxins have shown
activity against Coleopteran insects. The Sip toxin was
first reported from Bt strain EG2158 and was designated
as Sip1Aa1 (Donovan et al. 2006).
Induction of systemic resistance
It is an established fact that beneficial micro-organisms
can induce the activation of plant immune system to
temporarily confer the plants’ resistance towards patho-
gens and insects. Induced resistance is generally expressed
at the site of induction but it can be systemic with
expression in other plant parts. Hence, this is regarded as
ISR. Generally, induced resistance confers an increased
level of protection against a broad spectrum of biological
invaders (Pieterse et al. 2014). Unlike, systemic acquired
resistance which is triggered upon prior exposure of
pathogens or pests, microbe-mediated ISR is normally
orchestrated through JA and ET. However, recent reports
suggest that salicylic acid (SA) produced by Bacillus spp.
confers ISR to a wide variety of plants against diverse
biotic stresses. Rahman et al. (2015) deduced that B.
velezensis FZB42 conferred ISR in perennial rye grass
(Lolium perenne) against Magnaporthe oryzae which is
actuated through hydrogen peroxide burst, elevated per-
oxidase activity, and deposition of callose and phenolic/
polyphenolic compounds. Burkhanova et al. (2017)
reported SA-regulated ISR in B. subtilis and B. thuringien-
sis inoculated wheat against Septoria nodorum. Miao et al.
(2018) showed that Bacillus simplex elicited early plant
defence system in tobacco by increasing the production
of reactive oxygen species and callose deposition medi-
ated through both JA/ET and SA defence signalling net-
works. Bacillus cereus elicited the production of phenyl
ammonia lyase, polyphenol oxidase, etc. and conferred
ISR in loquat trees against Colletotrichum acutatum
(Wang et al. 2014). Zebelo et al. (2016) showed that
Bacillus spp. conferred protection in cotton against Spo-
doptera exigua through higher gossypol accumulation
which was again related with the activation of genes
involved in JA defence signalling network. Bacillus
velezensis YC7010-mediated ISR against brown plant hop-
per (Nilaparvata lugens) in rice was also actuated through
JA and SA-dependent defence pathways (Harun-Or-
Rashid et al. 2018). Transcriptome studies of rice revealed
that inoculation of B. velezensis YC7010 resulted in
upregulation of genes related to jasmonate-regulated pro-
teins like lipoxygenase, jacalin-related lectins, flavones
and phenolics which are known to play roles in
Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology
Bacillus sp. in soil and plant health
protection from herbivory. Apart from insects, Bacillus
spp. are also known to elicit ISR against nematodes and
viruses. Hu et al. (2018) reported that B. cereus BCM2
could induce ISR against Meloidogyne incognita in tomato
through upregulation of defensin-like proteins, ET
responsive transcription factors, WRKY transcription fac-
tors and defence enzymes. Bacillus velezensis 5B6 could
elicit ISR in pepper plants against cucumber mosaic virus
through upregulation of pathogenicity-related (PR) genes
(Lee and Ryu 2016). Similarly, Guo et al. (2019) reported
that B. velezensis Ba13 could show ISR in tomato against
tomato yellow leaf curl virus by enhancing the expression
of PR genes (PR1, PR2, PR3) and defence-related
enzymes.
Lytic enzymes
Due to their metabolic diversity, Bacillus spp. are known
to produce a number of lytic enzymes. Among these
enzymes, chitinases, b-1,3-glucanases, b-glucosidase,
lipases and proteases are of special importance as they
have the ability to degrade the components of fungal cell
wall such as chitin, b-glucans and proteins. A wide vari-
ety of Bacillus spp. like B. subtilis, B. thuringiensis, B.
licheniformis, B. safensis, B. pumilus, B. velezensis, B. cereus
etc. are known to produce chitinases (Berini et al. 2018).
Ghasemi et al. (2010) reported efficient chitinase from B.
pumilus SG2 which showed inhibitory effects on Fusar-
ium graminearum, Rhizoctonia solani, Magnaporthe grisea,
Botrytis cinerea, etc. Antifungal activity of B. licheniformis
against Phoma medicaginis has also been attributed to the
production of chitinase (Slimene et al. 2015). Bacillus
velezensis HYEB5-6 has been shown to control Col-
letotrichum gloeosporioides through damaging the cell wall
by the action of proteases and glucanases (Huang et al.
2017). Similarly, production of protease and b-1,3-glu-
canase by B. velezensis NJZJSB3 has been attributed as
one of the means to control Sclerotinia sclerotiorum caus-
ing stem rot of canola (Wu et al. 2014). Shrestha et al.
(2015) reported that high activity of chitinase, protease
and b-1,3-glucanase is responsible for the hyphal degen-
eration and rupture of Sclerotinia minor causing lettuce
drop disease. It has also been suggested that chitinase
activity can further enhance the activity of Cry toxins.
Ding et al. (2008) reported that B. thuringiensis express-
ing a recombinant cry1Ac gene having a fused tobacco
endochitinase showed 11
3 times higher toxicity against
H. armigera. Gonzalez-Ponce et al. (2017) also showed
that B. thuringiensis kurstaki HD-73 with fused chitinase
and Cry1Ac had higher toxicity against Spodoptera frugi-
perda as compared to native HD-73 strain. Insecticidal
activity due to disruption of periotrophic membrane has
also been attributed to chitinases alone.
1589
Bacillus sp. in soil and plant health
Volatile organic compounds
Microbial volatiles are typically small low-molecular
weight (0
1–0
5 kDa) compounds having up to 20 carbon
atoms with a lipophilic moiety, high vapour pressure and
low boiling point. Using headspace solid-phase microex-
traction combined with gas chromatography-mass spec-
trometry (HS-SPME-GC-MS), Gao et al. (2018)
identified 74 different volatile organic compounds (VOC)
from B. subtilis CF-3 of which ketone, acids, ethers and
phenols were predominant. Among these VOC, 2,4-di-
tert-butylthiophenol and benzothiazole had strong inhibi-
tory effect against Monilinia fructicola and C. gloeospori-
oides (Gao et al. 2018). Massawe et al. (2018) reported 16
different types of VOC from three different species of
Bacillus and eight of these VOC could inhibit the growth
of S. sclerotiorum. B. velezensis SQR-9 produced 22 differ-
ent VOC of which nine compounds showed antibacterial
activity against R. solanacearum (Raza et al. 2016). Tahir
et al. (2017) reported that B. velezensis FZB42 and B.
atrophaeus LSSC22 showing inhibitory effect against R.
solanacearum produce 13 and 10 different VOC respec-
tively. Li et al. (2015) profiled the VOC produced by
eight biocontrol strains belonging to different Bacillus
spp. and recorded 50 different VOC belonging to eight
classes like ketones (21), alcohols (11), aldehydes (5),
pyrazines (4), acids (3), esters (3), pyridines (2) and ben-
zene (1).
Biofilm formation
The two major mechanisms of action by biocontrol
agents against pathogens and pests as reported by many
in the past are the production of antimicrobial com-
pounds (ranging from antimicrobial metabolites to vola-
tile organic compounds, including lytic enzymes and
crystal proteins) and ISR. However, recent research in the
field of biocontrol has led to consideration of root colo-
nization and biofilm formation as one of the mechanisms
of biocontrol activity. Root colonization and biofilm for-
mation have been reported as a mechanism of biocontrol
in different species of Bacillus like B. velezensis, B. atro-
phaeus and B. subtilis (Pandin et al. 2017). Root exudates
of host plants and lipopeptides like bacillomycin and sur-
factin are known to induce biofilm formation in different
bacilli. Fan et al. (2011) have reported the formation of
biofilm by B. velezensis FZB42 in the roots of Zea mays,
A. thaliana and Lemna minor. Surfactin was found to
play an important role in colonization of roots and bio-
film formation by B. atrophaeus and B. subtilis. Root exu-
dates of cucumber were found to drive chemotaxis of B.
velezensis SQR9 and biofilm formation in the rhizosphere
by inducing the production of bacillomycin D (Pandin
1590 Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology
A.K. Saxena et al.
et al. 2017). Increasing evidence on the biofilm formation
in the rhizosphere and rhizoplane for biocontrol of
pathogens warrants more investigations.
Conclusion
Bacillus spp. are one of the predominant culturable soil
bacteria in majority of the soils and are well known for
their abilities to exert a wide variety of plant beneficial
effects. Due to their genetic and metabolic diversity,
Bacillus spp. are well-adapted to a wide range of environ-
mental conditions. Such a wide environmental adaptabil-
ity with multitude of beneficial traits make Bacillus spp. a
suitable candidate for their application as biofertilizer or
biocontrol agent. The traits of Bacillus spp. associated
with biological control are commercially more exploited
as evident from the wide range of applications of cry
genes. However, apart from the ability of the Bacillus spp.
to produce endotoxins, the features like production of
antimicrobial peptides should also be commercially
exploited after sufficient field trials. A number of com-
mercial formulations of Bacillus spp. showing different
nutrient mobilizing activities and phytohormone produc-
tion are also available globally. But their applicability in
terms of crops and geographical regions are very limited
even though reports on Bacillus as plant growth promoter
are much higher than any other bacteria. There is a need
to focus on the field application of the potential strains
of Bacillus which can be applied on a variety of crops
over a wide range of agro-climatic conditions. Interac-
tions between Bacillus and other soil micro-organisms are
also well-understood and have been exploited commer-
cially to some extent. The members of the genus Bacillus
hold tremendous potential for agro-biotechnological
applications due to their multifarious functional attri-
butes. However, the arena of practical utility needs to be
expanded through more focused research and testing for
crop productivity under field conditions.
Conflict of Interest
None declared.
References
Alina, S.O., Constantinscu, F. and Petrutßa, C.C. (2015)
Biodiversity of Bacillus subtilis group and beneficial traits
of Bacillus species useful in plant protection. Rom
Biotechnol Lett 20, 10737–10750.
Ambreetha, S., Chinnadurai, C., Marimuthu, P. and
Balachandar, D. (2018) Plant-associated Bacillus modulates
the expression of auxin-responsive genes of rice and
modifies the root architecture. Rhizosphere 5, 57–66.
A.K. Saxena et al.
Ambrico, A. and Trupo, M. (2017) Efficacy of cell free
supernatant from Bacillus subtilis ET-1, an Iturin A
producer strain, on biocontrol of green and gray mold.
PostHarvest Biol Technol 134, 5–10.
Ambrosini, A., Stefanski, T., Lisboa, B.B., Beneduzi, A.,
Vargas, L.K. and Passaglia, L.M.P. (2016) Diazotrophic
bacilli isolated from the sunflower rhizosphere and the
potential of Bacillus mycoides B38V as biofertiliser. Ann
Appl Biol 168, 93–110.
Asari, S., Tarkowska, D., Rol
cık, J., Novak, O., Palmero, D.V.,
Bejai, S., Bejai, S. and Meijer, J. (2017) Analysis of plant
growth-promoting properties of Bacillus amyloliquefaciens
UCMB5113 using Arabidopsis thaliana as host plant.
Planta 245, 15–30.
Babu, A.G., Kim, J.D. and Oh, B.T. (2013) Enhancement of
heavy metal phytoremediation by Alnus firma with
endophytic Bacillus thuringiensis GDB-1. J Hazard Mater
250, 477–483.
Basak, B.B. and Biswas, D.R. (2010) Co-inoculation of
potassium solubilizing and nitrogen fixing bacteria on
solubilization of waste mica and their effect on growth
promotion and nutrient acquisition by a forage crop. Biol
Fert Soils 46, 641–648.
Bashan, Y., de-Bashan, L.E., Prabhu, S.R. and Hernandez, J.P.
(2014) Advances in plant growth-promoting bacterial
inoculant technology: formulations and practical
perspectives (1998–2013). Plant Soil 378, 1–33.
Berini, F., Katz, C., Gruzdev, N., Casartelli, M., Tettamanti, G.
and Marinelli, F. (2018) Microbial and viral chitinases:
Attractive biopesticides for integrated pest management.
Biotechnol Adv 36, 818–838.
Bhattacharyya, P.N. and Jha, D.K. (2012) Plant growth-
promoting rhizobacteria (PGPR): emergence in
agriculture. World J Microbiol Biotechnol 28, 1327–1350.
Borriss, R., Wu, H. and Gao, X. (2019) Secondary metabolites
of the plant growth promoting model rhizobacterium
Bacillus velezensis FZB42 are involved in direct suppression
of plant pathogens and in stimulation of plant-induced
systemic resistance. In Secondary Metabolites of Plant
Growth Promoting Rhizomicroorganisms: Discovery and
Applications ed. Singh, H.B., Keswani, C., Reddy, M.S.,
Sansinenea, E. and Garcıa-Estrada, C. pp. 147–168.
Singapore: Springer.
Burkhanova, G.F., Veselova, S.V., Sorokan, A.V., Blagova,
D.K., Nuzhnaya, T.V. and Maksimov, I.V. (2017) Strains
of Bacillus ssp. regulate wheat resistance to Septoria
nodorum Berk. Appl Biochem Microbiol 53, 346–352.


Colo, J., Hajnal-Jafari, T.I., Duric, S., Stamenov, D. and
Hamidovic, S. (2014) Plant growth promotion
rhizobacteria in onion production. Polish J Microbiol 63,
83–88.
Crickmore, N., Baum, J., Bravo, A., Lereclus, D., Narva, K.,
Sampson, K., Schnepf, E., Sun, M.et al. (2015) Bacillus
thuringiensis toxin nomenclature 2014. http://www.lifesc
i.sussex.ac.uk/Home/Neil_Crickmore/Bt/
Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology
Bacillus sp. in soil and plant health
Ding, Y., Wang, J., Liu, Y. and Chen, S. (2005) Isolation and
identification of nitrogen-fixing bacilli from plant
rhizospheres in Beijing region. J Appl Microbiol 99, 1271–
1281.
Ding, X., Luo, Z., Xia, L., Gao, B., Sun, Y. and Zhang, Y.
(2008) Improving the insecticidal activity by expression of
a recombinant cry1Ac gene with chitinase-encoding gene
in acrystalliferous Bacillus thuringiensis. Curr Microbiol 56,
442–446.
Ding, X., Peng, X.J., Jin, B.S., Xiao, M., Chen, J.K., Li, B. and
Nie, M. (2015) Spatial distribution of bacterial
communities driven by multiple environmental factors in
a beach wetland of the largest freshwater lake in China.
Front Microbiol 6, 129.
Donovan, W.P., Engleman, J.T., Donovan, J.C., Baum, J.A.,
Bunkers, G.J., Chi, D.J. and Krasomil-Osterfeld, K.C.
(2006) Discovery and characterization of Sip1A: A novel
secreted protein from Bacillus thuringiensis with activity
against coleopteran larvae. Appl Microbiol Biotechnol 72,
713–719.
Falardeau, J., Wise, C., Novitsky, L. and Avis, T.J. (2013)
Ecological and mechanistic insights into the direct and
indirect antimicrobial properties of Bacillus subtilis
lipopeptides on plant pathogens. J Chem Ecol 39, 869–878.
Fan, B., Chen, X.H., Budiharjo, A., Bleiss, W., Vater, J. and
Borriss, R. (2011) Efficient colonization of plant roots by
the plant growth promoting bacterium Bacillus
amyloliquefaciens FZB42, engineered to express green
fluorescent protein. J Biotechnol 151, 303–311.
Fan, B., Wang, C., Song, X., Ding, X., Wu, L., Wu, H., Gao,
X. and Borriss, R. (2018) Bacillus velezensis FZB42 in
2018: The Gram-positive model strain for plant growth
promotion and biocontrol. Front Microbiol 9, 2491.
Farhat, A., Chouayekh, H., Farhat, M.B., Bouchaala, K. and
Bejar, S. (2008) Gene cloning and characterization of a
thermostable phytase from Bacillus subtilis US417 and
assessment of its potential as a feed additive in comparison
with a commercial enzyme. Mol Biotechnol 40, 127.
Fira, D., Dimkic, I., Beric, T., Lozo, J. and Stankovic, S. (2018)
Biological control of plant pathogens by Bacillus species. J
Biotechnol 285, 44–55.
Flissi, A., Dufresne, Y., Michalik, J., Tonon, L., Janot, S., Noe,
L. and Pupin, M. (2016) Norine, the knowledgebase
dedicated to non-ribosomal peptides, is now open to
crowdsourcing. Nucleic Acids Res 44, D1113–D1118.
Freitas, M.A., Medeiros, F.H.V., Carvalho, S.P., Guilherme,
L.R.G., Teixeira, W.D., Zhang, H. and Pare, P. (2015)
Augmenting iron accumulation in cassava by the
beneficial soil bacterium Bacillus subtilis (GBO3). Front
Plant Sci 6, 596.
Gao, H., Li, P., Xu, X., Zeng, Q. and Guan, W. (2018)
Research on volatile organic compounds from Bacillus
subtilis CF-3: biocontrol effects on fruit fungal pathogens
and dynamic changes during fermentation. Front Microbiol
9, 456.
1591
Bacillus sp. in soil and plant health
Ghasemi, S., Ahmadian, G., Jelodar, N.B., Rahimian, H.,
Ghandili, S., Dehestani, A. and Shariati, P. (2010)
Antifungal chitinases from Bacillus pumilus SG2: Preliminary
report. World J Microbiol Biotechnol 26, 1437–1443.
Glick, B.R. (2014) Bacteria with ACC deaminase can promote
plant growth and help to feed the world. Microbiol Res
169, 30–39.
Gonzalez-Ponce, K.S., Casados-Vazquez, L.E., Salcedo-
Hernandez, R., Bideshi, D.K., del Rinc on-Castro, M.C.
and Barboza-Corona, J.E. (2017) Recombinant Bacillus
thuringiensis subsp. kurstaki HD73 strain that synthesizes
Cry1Ac and chimeric ChiA74Δsp chitinase inclusions.
Arch Microbiol 199, 627–633.
Goswami, D., Dhandhukia, P., Patel, P. and Thakker, J.N.
(2014) Screening of PGPR from saline desert of Kutch:
growth promotion in Arachis hypogea by Bacillus
licheniformis A2. Microbiol Res 169, 66–75.
Goswami, D., Thakker, J.N. and Dhandhukia, P.C. (2016)
Portraying mechanics of plant growth promoting
rhizobacteria (PGPR): a review. Cogent Food Agric 2,
1127500.
Guang-Can, T.A.O., Shu-Jun, T., Miao-Ying, C.A.I. and
Guang-Hui, X.I.E. (2008) Phosphate-solubilizing and
mineralizing abilities of bacteria isolated from soils.
Pedosphere 18, 515–523.
Guo, Q., Dong, W., Li, S., Lu, X., Wang, P., Zhang, X., Wang,
Y. and Ma, P. (2014) Fengycin produced by Bacillus
subtilis NCD-2 plays a major role in biocontrol of cotton
seedling damping-off disease. Microbiol Res 169, 533–540.
Guo, Q., Li, Y., Lou, Y., Shi, M., Jiang, Y., Zhou, J. and Lai,
H. (2019) Bacillus amyloliquefaciens Ba13 induces plant
systemic resistance and improves rhizosphere
microecology against tomato yellow leaf curl virus disease.
Appl Soil Ecol 137, 154–166.
Habibi, S., Djedidi, S., Prongjunthuek, K., Mortuza, M.F.,
Ohkama-Ohtsu, N., Sekimoto, H. and Yokoyoma, T.
(2014) Physiological and genetic characterization of rice
nitrogen fixer PGPR isolated from rhizosphere soils of
different crops. Plant Soil 379, 51–66.
Harun-Or-Rashid, M., Kim, H.J., Yeom, S.I., Yu, H.A., Manir,
M.M., Moon, S.S. and Chung, Y.R. (2018) Bacillus
velezensis YC7010 enhances plant defenses against brown
planthopper through transcriptomic and metabolic
changes in rice. Front Plant Sci 9, 1904.
Hu, H., Wang, C., Li, X., Tang, Y., Wang, Y., Chen, S. and
Yan, S. (2018) RNA-Seq identification of candidate
defense genes targeted by endophytic Bacillus cereus-
mediated induced systemic resistance against Meloidogyne
incognita in tomato. Pest Manag Sci 74, 2793–2805.
Huang, L., Li, Q.C., Hou, Y., Li, G.Q., Yang, J.Y., Li, D.W.
and Ye, J.R. (2017) Bacillus velezensis strain HYEB5-6 as a
potential biocontrol agent against anthracnose on
Euonymus japonicus. Biocontrol Sci Technol 27, 636–653.
Ibarra-Galeana, J.A., Castro-Martınez, C., Fierro-Coronado,
R.A., Armenta-Boj orquez, A.D. and Maldonado-Mendoza,
1592 Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology
A.K. Saxena et al.
I.E. (2017) Characterization of phosphate-solubilizing
bacteria exhibiting the potential for growth promotion
and phosphorus nutrition improvement in maize (Zea
mays L.) in calcareous soils of Sinaloa, Mexico. Ann
Microbiol 67, 801–811.
Ji, S.H., Gururani, M.A. and Chun, S.C. (2014) Isolation and
characterization of plant growth promoting endophytic
diazotrophic bacteria from Korean rice cultivars. Microbiol
Res 169, 83–98.
Kang, S.M., Radhakrishnan, R., You, Y.H., Joo, G.J., Lee, I.J.,
Lee, K.E. and Kim, J.H. (2014) Phosphate solubilizing
Bacillus megaterium mj1212 regulates endogenous plant
carbohydrates and amino acids contents to promote
mustard plant growth. Indian J Microbiol 54, 427–433.
Kumawat, N., Kumar, R., Kumar, S. and Meena, V.S. (2017)
Nutrient solubilizing microbes (NSMs): its role in
sustainable crop production Bt-agriculturally important
microbes for sustainable agriculture. In Applications in
Crop Production and Protection ed. Meena, V.S., Mishra,
P.K., Bisht, J.K. and Pattanayak, A. vol. 2, pp. 25–61.
Singapore: Springer.
Lee, G.H. and Ryu, C.M. (2016) Spraying of leaf-colonizing
Bacillus amyloliquefaciens protects pepper from cucumber
mosaic virus. Plant Dis 100, 2099–2105.
Li, B., Li, Q., Xu, Z., Zhang, N., Shen, Q. and Zhang, R.
(2014) Responses of beneficial Bacillus amyloliquefaciens
SQR9 to different soilborne fungal pathogens through the
alteration of antifungal compounds production. Front
Microbiol 5, 636.
Li, X.Y., Mao, Z.C., Wu, Y.X., Ho, H.H. and He, Y.Q. (2015)
Comprehensive volatile organic compounds profiling of
Bacillus species with biocontrol properties by head space
solid phase microextraction with gas chromatography-
mass spectrometry. Biocontrol Sci Technol 25, 132–143.
Lim, J.H. and Kim, S.D. (2009) Synergistic plant growth
promotion by the indigenous auxins-producing PGPR
Bacillus subtilis AH18 and Bacillus licheniforims K11. J
Korean Soc Appl Biol Chem 52, 531–538.
Lim, J.H. and Kim, S.D. (2013) induction of drought stress
resistance by multi-functional PGPR Bacillus licheniformis
K11 in pepper. Plant Pathol J 29, 201–208.
Madhaiyan, M., Poonguzhali, S., Lee, J.S., Lee, K.C. and Hari,
K. (2011) Bacillus rhizosphaerae sp. nov., a novel
diazotrophic bacterium isolated from sugarcane
rhizosphere soil. Antonie Van Leeuwenhoek van
Leeuwenhoek 100, 437–444.
Massawe, V.C., Rao, A.H., Farzand, A., Mburu, D.K., Ochola,
S.O., Wu, L. and Gao, X. (2018) Volatile organic
compounds of endophytic Bacillus spp. have biocontrol
activity against Sclerotinia sclerotiorum. Phytopathology 108,
1373–1385.
Mehta, P., Walia, A., Chauhan, A., Kulshrestha, S. and
Shirkot, C.K. (2013) Phosphate solubilisation and plant
growth promoting potential by stress tolerant Bacillus sp.
isolated from rhizosphere of apple orchards in trans
A.K. Saxena et al.
Himalayan region of Himachal Pradesh. Ann Appl Biol
163, 430–443.
Mehta, P., Walia, A., Kulshrestha, S., Chauhan, A. and
Shirkot, C.K. (2015) Efficiency of plant growth-promoting
P-solubilizing Bacillus circulans CB7 for enhancement of
tomato growth under net house conditions. J Basic
Microbiol 55, 33–44.
Miao, G.P., Han, J., Wang, C.R., Zhang, K.G. and Wang, S.C.
(2018) Growth inhibition and induction of systemic
resistance against Pythium aphanidermatum by Bacillus
simplex strain HS-2. Biocontrol Sci Technol 28, 1114–1127.
Mora, I., Cabrefiga, J. and Montesinos, E. (2015) Cyclic
lipopeptide biosynthetic genes and products, and
inhibitory activity of plant-associated Bacillus against
phytopathogenic bacteria. PLoS ONE 10, e0127738.
Mukhtar, S., Shahid, I., Mehnaz, S. and Malik, K.A. (2017)
Assessment of two carrier materials for phosphate
solubilizing biofertilizers and their effect on growth of
wheat (Triticum aestivum L.). Microbiol Res 205, 107–117.
Murthy, K.S., Vineela, V. and Devi, P.S.V. (2014) Generation
of nanoparticles from technical powder of the insecticidal
bacterium Bacillus thuringiensis var. kurstaki for improving
efficacy. Int Biomed Nanosci Nanotechnol 33, 236–250.
Palma, L., Mu~ noz, D., Berry, C., Murillo, J., Caballero, P. and
Caballero, P. (2014) Bacillus thuringiensis toxins: an
overview of their biocidal activity. Toxins 6, 3296–3325.
Panda, B., Rahman, H. and Panda, J. (2016) Phosphate
solubilizing bacteria from the acidic soils of Eastern
Himalayan region and their antagonistic effect on fungal
pathogens. Rhizosphere 2, 62–71.
Pandin, C., Le Coq, D., Canette, A., Aymerich, S. and
Briandet, R. (2017) Should the biofilm mode of life be
taken into consideration for microbial biocontrol agents?
Microb Biotechnol 10, 719–734.
Park, Y.G., Mun, B.G., Kang, S.M., Hussain, A., Shahzad, R.,
Seo, C.W. and Lee, I.J. (2017) Bacillus aryabhattai SRB02
tolerates oxidative and nitrosative stress and promotes the
growth of soybean by modulating the production of
phytohormones. PLoS ONE 12, e0173203.
Passari, A.K., Lalsiamthari, P.C., Leo, V.V., Mishra, V.K.,
Yadav, M.K., Gupta, V.K. and Singh, B.P. (2018)
Biocontrol of Fusarium wilt of Capsicum annuum by
rhizospheric bacteria isolated from turmeric endowed with
plant growth promotion and disease suppression potential.
Eur J Plant Pathol 150, 831–846.
Pieterse, C.M., Zamioudis, C., Berendsen, R.L., Weller, D.M.,
Van Wees, S.C.M. and Bakker, P.A.H.M. (2014) Induced
systemic resistance by beneficial microbes. Annu Rev
Phytopathol 52, 347–375.
Pradhan, M., Dhali, S. and Lakra, P.B. (2018) Study on P
solubilizing efficiencies of native PSB isolates from acid
soils of Odisha. J Pharma Phyto 7, 1557–1566.
Pramanik, P., Goswami, A.J., Ghosh, S. and Kalita, C. (2019)
An indigenous strain of potassium-solubilizing bacteria
Bacillus pseudomycoides enhanced potassium uptake in tea
Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology
Bacillus sp. in soil and plant health
plants by increasing potassium availability in the mica
waste-treated soil of North-east India. J Appl Microbiol
126, 215–222.
Radhakrishnan, R. and Lee, I.J. (2016) Gibberellins producing
Bacillus methylotrophicus KE2 supports plant growth and
enhances nutritional metabolites and food values of
lettuce. Plant Physiol Biochem 109, 181–189.
Raheem, A., Shaposhnikov, A., Belimov, A.A., Dodd, I.C. and
Ali, B. (2018) Auxin production by rhizobacteria was
associated with improved yield of wheat (Triticum
aestivum L.) under drought stress. Arch Agron Soil Sci 64,
574–587.
Rahman, A., Uddin, W. and Wenner, N.G. (2015) Induced
systemic resistance responses in perennial ryegrass against
Magnaporthe oryzae elicited by semi-purified surfactin
lipopeptides and live cells of Bacillus amyloliquefaciens.
Mol Plant Pathol 16, 546–558.
Ramadoss, D., Lakkineni, V.K., Bose, P., Ali, S. and
Annapurna, K. (2013) Mitigation of salt stress in wheat
seedlings by halotolerant bacteria isolated from saline
habitats. SpringerPlus 2, 6.
Ramesh, A., Sharma, S.K., Sharma, M.P., Yadav, N. and Joshi,
O.P. (2014) Inoculation of zinc solubilizing Bacillus
aryabhattai strains for improved growth, mobilization and
biofortification of zinc in soybean and wheat cultivated in
Vertisols of central India. Appl Soil Ecol 73, 87–96.
Rao, W., Zhan, Y., Chen, S., Xu, Z., Huang, T., Hong, X. and
Guan, X. (2018) Flowerlike Mg(OH)2 cross-nanosheets for
controlling Cry1Ac protein loss: Evaluation of insecticidal
activity and biosecurity. J Agric Food Chem 66, 3651–3657.
Raza, W., Ling, N., Yang, L., Huang, Q. and Shen, Q. (2016)
Response of tomato wilt pathogen Ralstonia solanacearum
to the volatile organic compounds produced by a
biocontrol strain Bacillus amyloliquefaciens SQR-9. Sci Rep
6, 24856.
Roh, J.Y., Choi, J.Y., Li, M.S., Jin, B.R. and Je, Y.H. (2007)
Bacillus thuringiensis as a specific, safe, and effective tool
for insect pest control. J Microbiol Biotechnol 17, 547.
Saeid, A., Prochownik, E. and Dobrowolska-Iwanek, J. (2018)
Phosphorus solubilization by Bacillus species. Molecules 23,
2897.
Saha, M., Maurya, B.R., Meena, V.S., Bahadur, I. and Kumar,
A. (2016) Identification and characterization of potassium
solubilizing bacteria (KSB) from Indo-Gangetic plains of
India. Biocatal Agric Biotechnol 7, 202–209.
Saxena, A.K., Karthikeyan, N. and Rajawat, M.V.S. (2017)
Microbial interventions for improving phosphorus and
potassium nutrition in plants. Indian J Fertilisers 13, 128–
137.
Shakeel, M., Rais, A., Hassan, M.N. and Hafeez, F.Y. (2015)
Root Associated Bacillus sp. improves growth, yield and
zinc translocation for basmati rice (Oryza sativa) varieties.
Front Microbiol 6, 1286.
Sharma, S.B., Sayyed, R.Z., Trivedi, M.H. and Gobi, T.A.
(2013) Phosphate solubilizing microbes: sustainable
1593
Bacillus sp. in soil and plant health
approach for managing phosphorus deficiency in
agricultural soils. Springerplus 2, 587.
Shim, J., Kim, J.W., Shea, P.J. and Oh, B.T. (2015) IAA
production by Bacillus sp. JH 2–2 promotes Indian
mustard growth in the presence of hexavalent chromium.
J Basic Microbiol 55, 652–658.
Shrestha, A., Sultana, R., Chae, J.C., Kim, K. and Lee, K.J.
(2015) Bacillus thuringiensis C25 which is rich in cell wall
degrading enzymes efficiently controls lettuce drop caused
by Sclerotinia minor. Eur J Plant Pathol 142, 577–589.
Singh, N.P., Singh, R.K., Meena, V.S. and Meena, R.K. (2015)
Can we use maize (Zea mays) rhizobacteria as plant
growth promoter. Vegetos 28, 86–99.
Singh, D., Rajawat, M.V.S., Kaushik, R., Prasanna, R. and
Saxena, A.K. (2017) Beneficial role of endophytes in
biofortification of Zn in wheat genotypes varying in
nutrient use efficiency grown in soils sufficient and
deficient in Zn. Plant Soil 416, 107–116.
Slimene, I.B., Tabbene, O., Gharbi, D., Mnasri, B., Schmitter,
J.M., Urdaci, M.C. and Limam, F. (2015) Isolation of a
chitinolytic Bacillus licheniformis S213 strain exerting a
biological control against Phoma medicaginis infection.
Appl Biochem Biotechnol 175, 3494–3506.
Stein, T. (2005) Bacillus subtilis antibiotics: structures, syntheses
and specific functions. Mol Microbiol 56, 845–857.
Tahir, H.A.S., Gu, Q., Wu, H., Niu, Y., Huo, R. and Gao, X.
(2017) Bacillus volatiles adversely affect the physiology and
ultra-structure of Ralstonia solanacearum and induced
systemic resistance in tobacco against bacterial wilt. Sci
Rep 7, 40481.
Van Elsas, J.D., Trevors, J.T., Jansson, J.K. and Nannipieri, P.
(2006) Modern Soil Microbiology. Boca Raton, FL: CRC Press.
Verma, P., Yadav, A.N., Khannam, K.S., Panjiar, N., Kumar,
S., Saxena, A.K. and Suman, A. (2015) Assessment of
genetic diversity and plant growth promoting attributes of
psychrotolerant bacteria allied with wheat (Triticum
aestivum) from the northern hills zone of India. Ann
Microbiol 65, 1885–1899.
Vinci, G., Cozzolino, V., Mazzei, P., Monda, H., Savy, D.,
Drosos, M. and Piccolo, A. (2018) Effects of Bacillus
amyloliquefaciens and different phosphorus sources on
Maize plants as revealed by NMR and GC-MS based
metabolomics. Plant Soil 429, 437–450.
Vineela, V., Nataraj, T., Reddy, G. and Vimala Devi, P.S.
(2017) Enhanced bioefficacy of Bacillus thuringiensis var.
kurstaki against Spodoptera litura (Lepidoptera: Noctuidae)
through particle size reduction and formulation as a
suspension concentrate. Biocontrol Sci Technol 27, 58–69.
1594 Journal of Applied Microbiology 128, 1583--1594 © 2019 The Society for Applied Microbiology
A.K. Saxena et al.
Wang, X., Wang, L., Wang, J., Jin, P., Liu, H. and Zheng, Y.
(2014) Bacillus cereus AR156-induced resistance to
Colletotrichum acutatum is associated with priming of
defense responses in loquat fruit. PLoS ONE 11, e0112494.
Wu, Y., Yuan, J., Raza, W., Shen, Q. and Huang, Q. (2014)
Biocontrol traits and antagonistic potential of Bacillus
amyloliquefaciens strain NJZJSB3 against Sclerotinia
sclerotiorum, a causal agent of canola stem rot. J Microbiol
Biotechnol 24, 1327–1336.
Xu, M., Sheng, J., Chen, L., Men, Y., Gan, L., Guo, S. and
Shen, L. (2014) Bacterial community compositions of
tomato (Lycopersicum esculentum Mill.) seeds and plant
growth promoting activity of ACC deaminase producing
Bacillus subtilis (HYT-12-1) on tomato seedlings. World J
Microbiol Biotechnol 30, 835–845.
Yanez-Mendizabal, V., Zeriouh, H., Vi~ nas, I., Torres, R., Usall,
J., de Vicente, A. and Teixid o, N. (2012) Biological
control of peach brown rot (Monilinia spp.) by Bacillus
subtilis CPA-8 is based on production of fengycin-like
lipopeptides. Eur J Plant Pathol 132, 609–619.
Yousuf, J., Thajudeen, J., Rahiman, M., Krishnankutty, S.P.,
Alikunj, A., and A Abdulla, M.H. (2017) Nitrogen fixing
potential of various heterotrophic Bacillus strains from a
tropical estuary and adjacent coastal regions. J Basic
Microbiol 57, 922–932.
Yuan, S., Wang, L., Wu, K., Shi, J., Wang, M., Yang, X. and
Shen, B. (2014) Evaluation of Bacillus-fortified organic
fertilizer for controlling tobacco bacterial wilt in
greenhouse and field experiments. Appl Soil Ecol 75, 86–
94.
Zaheer, A., Malik, A., Sher, A., Qaisrani, M.M., Mehmood, A.,
Ullah Khan, S. and Rasool, M. (2019) Isolation,
characterization, and effect of phosphate-zinc-solubilizing
bacterial strains on chickpea (Cicer arietinum L.) growth.
Saudi J Biol Sci 26, 1061–1067.
Zahir, Z.A., Ahmad, M., Hilger, T.H., Dar, A., Malik, S.R.,
Abbas, G. and Rasche, F. (2018) Field evaluation of
multistrain biofertilizer for improving the productivity of
different mungbean genotypes. Soil Environ 37, 45–52.
Zebelo, S., Song, Y., Kloepper, J.W. and Fadamiro, H. (2016)
Rhizobacteria activates cadinene synthase genes and
induces systemic resistance in cotton against beet
armyworm (Spodoptera exigua). Plant Cell Environ 39,
935–943.
Zhao, X. and Kuipers, O.P. (2016) Identification and
classification of known and putative antimicrobial
compounds produced by a wide variety of Bacillales
species. BMC Genom 17, 882.