Bacillus Subtilis Impact On Plant Growth, Soil Health and

Received: 30 December 2021
| Accepted: 4 February 2022
DOI: 10.1111/jam.15480
REVIEW ARTICLE
Bacillus subtilis impact on plant growth, soil health and

environment: Dr. Jekyll and Mr. Hyde
Subhasmita Mahapatra | Radheshyam Yadav | Wusirika Ramakrishna
Department of Biochemistry, Central Abstract

University of Punjab, Bathinda, India
The increased dependence of farmers on chemical fertilizers poses a risk to soil fertil-
Correspondence ity and ecosystem stability. Plant growth-promoting rhizobacteria (PGPR) are at the
Wusirika Ramakrishna, Department forefront of sustainable agriculture, providing multiple benefits for the enhancement
of Biochemistry, Dean In-Charge
Academics, Dean, School of Basic
of crop production and soil health. Bacillus subtilis is a common PGPR in soil that
Sciences, Central University of Punjab, plays a key role in conferring biotic and abiotic stress tolerance to plants by induced
Ghudda, Bathinda, Punjab 151401, systemic resistance (ISR), biofilm formation and lipopeptide production. As a part of
India.
Email: [email protected]; bioremediating technologies, Bacillus spp. can purify metal contaminated soil. It acts
[email protected] as a potent denitrifying agent in agroecosystems while improving the carbon seques-
tration process when applied in a regulated concentration. Although it harbours sev-
eral antibiotic resistance genes (ARGs), it can reduce the horizontal transfer of ARGs
during manure composting by modifying the genetic makeup of existing microbiota.
In some instances, it affects the beneficial microbes of the rhizosphere. External in-
oculation of B. subtilis has both positive and negative impacts on the endophytic and
semi-synthetic microbial community. Soil texture, type, pH and bacterial concentra-
tion play a crucial role in the regulation of all these processes. Soil amendments and
microbial consortia of Bacillus produced by microbial engineering could be used to
lessen the negative effect on soil microbial diversity. The complex plant–microbe
interactions could be decoded using transcriptomics, proteomics, metabolomics and
epigenomics strategies which would be beneficial for both crop productivity and the
well-being of soil microbiota. Bacillus subtilis has more positive attributes similar to
the character of Dr. Jekyll and some negative attributes on plant growth, soil health
and the environment akin to the character of Mr. Hyde.
KEYWORDS
antibiotic resistance genes, Bacillus consortia, PGPR, plant-microbe interaction, sustainable
agriculture
I N T RO DU CT ION (Ramakrishna et al., 2019). Continuous and indiscrimi-

nate use of chemicals adversely affects human and ani-
The excessive use of chemical fertilizers in current ag- mal health by accumulating in the crops and entering the
ricultural practices deteriorates soil quality, contam- food chain through the biomagnification process (Naik
inates groundwater and poses a risk to biodiversity et al., 2019). Considering all the scenarios of modern
Subhasmita Mahapatra and Radheshyam Yadav contributed equally for this work.
J Appl Microbiol. 2022;132:3543–3562. wileyonlinelibrary.com/journal/jam © 2022 Society for Applied Microbiology. | 3543
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13652672, 2022, 5, Downloaded from https://enviromicro-journals.onlinelibrary.wiley.com/doi/10.1111/jam.15480 by INASP - TANZANIA, Wiley Online Library on [09/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
3544 MAHAPATRA et al.
agricultural practices, organic farming, and traditional ag- ammonia gases (Sun et al., 2020a). It plays a crucial role
ricultural methods, the use of biofertilizers is essential for in the regulation of the biogeochemical cycles providing
a sustainable agroecosystem. soil with a proper aeration capacity to maintain its eco-
Healthy soil maintenance depends upon certain pa- system. The presence of membrane efflux pumps and
rameters like carbon content, water filtration ability, oxy- BceAB type transporters in B. subtilis provide intrinsic re-
gen holding capacity, erosion minimization and microbial sistance against a broad range of antibiotics (Rismondo &
species diversity (Parray & Shameem, 2020). Chemical fer- Schulz, 2021). Though it can reduce the concentration of
tilizers induce plant growth but negatively impact all the other antibiotic resistance genes (ARGs) and mobile ge-
above factors resulting in loss of soil fertility. Application of netic elements from composting manure, its higher con-
plant growth-promoting rhizobacteria (PGPR) in agricul- centration affects other beneficial properties. Very little
ture is an alternative to reduce or replace chemical fertil- information is present about the horizontal transfer of
izers and improve soil fertility (Ramakrishna et al., 2019). ARGs and their significance in agriculture. Although B.
PGPR can be exploited as an efficient tool to induce plant subtilis is considered a beneficial microbe, sometimes it
growth in stress conditions. They can interact with plants affects the endophytic and rhizospheric microbiota neg-
directly for enhancement of nutrient uptake (macro and atively by decreasing their number and modifying the
micronutrients), phytohormone production, regulation of genetic makeup (US EPA, 1997). It depends on soil tex-
stress hormones and enzymes such as ethylene, abscisic ture, composition, pH and bacterial concentration in the
acid (ABA), 1-aminocyclopropane 1-carboxylase (ACC) rhizosphere. Therefore, it is essential to perform a feasi-
deaminase, and indirectly by biocontrol activity against bility study before applying microbial inoculants in the
pathogens through intraspecific interaction, cell wall soil. Several omics technologies (genomics, epigenomics,
lysing enzyme secretion, lipopeptides production and in- transcriptomics, proteomics, metabolomics) are available
duced systemic resistance (ISR) (Ramakrishna et al., 2020; for the functional and structural assessment and charac-
Yadav et al., 2020; Yadav et al., 2021). terization of bacterial diversity. Preparation of microbial
Bacillus subtilis is a common PGPR present in rhizo- inoculants by genetic engineering with no effect on other
sphere. The spores produced by Bacillus are long-lived microbial communities would benefit both the plant and
and sustain several harsh environmental conditions; thus microbe. Even after the successful application of micro-
can be employed in diverse growth conditions (Nicholson bial consortia as biofertilizers during experimental trials,
et al., 2000). It is one of the prominent biofilm-forming some of them fail to reach farmer’s satisfaction in the field
rhizobacteria, which help plants in nutrient uptake and (Soumare et al., 2020). Thus, proper storage and transport
root colonization (Figure 1). The use of Bacillus inoc- of biofertilizers are required for increasing their field ef-
ulants in farmlands reduces the release of nitrogen and ficiency and shelf life. The objective of this review is to
F I G U R E 1 Impact of Bacillus subtilis on plant growth, soil health improvement and its environmental effects. Bacillus subtilis regulates
the stress responses of plants by several hormonal and enzymatic mechanisms where induced systemic resistance (ISR), lipopeptide and
biofilm formation. It plays a vital role in soil remediation and as a denitrifying agent in agriculture. It reduces the spread of antibiotic
resistance genes and mobile genetic elements. Even after having a plethora of positive effects, B. subtilis has some negative impact on the
rhizosphere and endophytic microbial community, which cannot be ignored. The concentration of bacteria plays an important role in
maintaining the biogeochemical cycles like carbon cycle and its sequestration process
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POSITIVE AND NEGATIVE EFFECTS OF BACILLUS SUBTILIS 3545
highlight both the positive and negative effects of B. sub- RNA polymerase (Schäfer & Turgay, 2019). In addition,
tilis taking into account recent research in this field and alarmones, secondary messengers of nutrient starva-
recommendations for a future road map for their efficient tion, act as efficient intermediates to counter heat shock
application in enhancing crop productivity. and other stresses (Schäfer et al., 2020). Endophytic spe-
cies are more effective as compared to epiphytic ones.
Inoculation of arbuscular mycorrhizal fungi (AMF) along
KE Y P L AY E R IN PLAN T G ROW TH with B. subtilis in the Talh tree has shown a synergistic ef-
P RO M OT I O N AN D N U T R IE N T S fect in ameliorating the adverse effects of salinity stress on
ACQ U I S I T I ON plant metabolism by producing glycine, betaine and pro-
line (Hashem et al., 2016). Bacillus spp. harbour several
Growth-promoting traits genes’ KatA, SodA, trxA and perR associated with protect-
ing the plants from oxidative stress (Zubair et al., 2019).
Plants encounter both biotic and abiotic stress in differ- Similarly, Bacillus spp. induce the expression of DegS,
ent stages of their lifetime. Studies have revealed that dpsU20, desk, desR and ResD which mitigates cold stress
inoculation of certain bacteria instead of chemical ferti- in plants through signal transduction pathways. Several
lizers would be beneficial for both the plant and microbe osmotic regulatory genes OpuAC and ohR were identified
world (Ramakrishna et al., 2020). Bacillus subtilis, a plant in psychotropic Bacillus strains which have a role in main-
growth-promoting bacterium, acts synergistically with the taining osmotic homeostasis in plants. They also improve
host plant in regulating its physiochemical processes by plant survival under abiotic stress by inducing the expres-
producing different volatile organic compounds (VOCs). sion of peroxidase (POD) enzymes thereby minimizing
Using gas chromatography–mass spectroscopy analysis, the negative effect caused by adverse agroclimatic condi-
scientists have observed that VOCs like albuterol and tions. Thus, regulating abiotic stress responses of plants
1,3-
propanediol, produced by B. subtilis SYST2, medi- using Bacillus species could improve global agricultural
ate plant growth promotion by upregulating the photo- productivity.
synthetic activity and phytohormone production (Tahir
et al., 2017). The endospore-producing Bacillus spp. tend
to survive for a longer period in soil and promote plant Phytohormones
growth more efficiently compared to other plant growth-
promoting bacteria (PGPB) that do not produce en- Bacillus spp. act as biostimulants through the production
dospores (Yadav et al., 2020, 2021). Furthermore, it was of phytohormones, auxin and cytokinin as well as expansin
reported that Bacillus spp. improves the photosynthetic that contribute to plant growth and development (Zubair
capacity of wheat plants as they produce siderophores et al., 2019). The presence of ACC deaminase genes in
which chelate iron and supply iron required for photosyn- Bacillus spp. confers the ability to lower the ethylene level
thetic machinery. Bacillus spp. reduce the iron deficiency in plants thereby enhancing growth and drought toler-
in plants and mitigate the heavy metal induced oxidative ance in treated plants (Gowtham et al., 2020). Similarly,
stress as they protect the indole-3-acetic acid (IAA) from VOCs such as 2-ethyl hexanol, tetrahydrofuran-3-ol and
oxidative damage (Ferreira et al., 2019). Previously, it was 2-heptanone belonging to alcohols, ketones, furans, terpe-
documented that siderophore producing Bacillus spp. in nes and sulphur compounds elicit plant growth through
combination with mycorrhizal fungi enhance the nutrient interaction with multiple compounds (Jiang et al., 2019).
acquisition in wheat grain and root tissues (Yadav et al., VOCs emitted by Bacilllus spp. significantly enhanced the
2021). Siderophore produced by these microbes in the endogenous auxin level and decreased the strigolactones
rhizosphere solubilize the unavailable forms of various level indicating that VOCs act as signalling molecules
nutrients via acidification. Furthermore, plants acquire modulating the regulatory pathways in associated plants.
the nutrients from the nutrient–siderophore complexes The crosstalk between auxin and strigolactones (SLs) pro-
using root-mediated processes like chelate degradation or motes plant growth induced by VOCs emitted by Bacillus
ligand exchange reaction (Rajkumar et al., 2010). spp. Cytokinins (CK) produced by Bacillus spp. are asso-
Abiotic stress has a negative effect on plant growth ciated with cell division, photomorphogenic development
and development. Bacillus subtilis has a high resilience to- and shoot differentiation. Likewise, gibberellins play a
wards abiotic stress due to its genomic organization and significant role in seed germination, flower initiations and
metabolic capabilities (Table 1). It harbours numerous fruit development. Bacillus spp. could be exploited as an
genes for plant growth promotion and abiotic stress con- alternative to obtain these phytohormones to enhance ag-
trol (Leontidou et al., 2020). Spx acts as the central regu- ricultural crop productivity. These microbes produce the
lator of stress control by binding to the alpha subunit of CKs, zeatin (Z), zeatin nucleotide (ZN) such as izopentyl
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TABLE 1 Bacillus subtilis mediated abiotic stress tolerance in plants
Abiotic stress Strain Plant Mechanism Reference

Drought B26 Brachypodium Upregulation of drought response genes DREB2B Gagné-Bourque et al. (2015)
distachyon like; modulation of DNA methylation genes
Drought B26 Timothy Accumulation of osmolyte in shoot and root Gagné-Bourque et al. (2016)
(GABA)
Drought RJ14 Pisum sativum Upregulation of ACC deaminase; downregulation Saikia et al. (2018)
Vigna mungo of ACC oxidase gene
Drought ………. Chick pea (Cicer Significant accumulation of nicotinamide and Khan et al. (2019)
arietinum) 4-hydroxy methyl glycine
Drought HAS31 Potato Maintenance of catalase, peroxidase and Batool et al. (2020)
superoxide dismutase enzymes
Drought 10-4 Wheat Decrease in lipid peroxidation; electrolyte leakage Lastochkina et al. (2020)
from tissues
Salt EGY16 Thymus vulgaris Decrease concentration of antioxidant enzymes Abdelshafy Mohamad
et al. (2020)
Salt GB03 White clover Regulation of plant chlorophyll content, cell Han et al. (2014)
membrane integrity, leaf osmotic potential,
ionic balance
Salt 10-4 Wheat Slow down statolite starch hydrolysis Lastochkina et al. (2017)
Salt SU47 Wheat Reducing the concentration of antioxidant Upadhyay et al. (2012)
enzymes
Salt BERA 71 Acacia gerradii Modulating osmotolerant system and antioxidant Hashem et al. (2016)
Benth. enzyme system
Salt NRCB003 Medicago sativa L. Increasing ACC deaminase activity Zhu et al. (2020)
Salt QST-713 Tomato ------------- Medeiros and Bettiol (2021)
Lead (Pb) FBL-10 Solanum Activate antioxidant system of plants; decrease Shah et al. (2021)
Toxicity melongena the level of peroxide and malondialdehyde
(MDA)
Iron (Fe) STU-6 Tomato Enhancement of polyamine mediated iron Zhou et al. (2019)
deficiency remobilization
Cadmium stress MF497446 Cow pea Produce IAA, GA and siderophores to induce El-Nahrawy et al. (2019)
plant growth under Cd stress
Cd, Cr, Ni KP717559 Brassica juncea Enhance phytoextraction by plants while Ndeddy Aka and
producing IAA, GA, HCN for plant growth Babalola (2016)
As, Cd, Cu, Ni KUJM2 Lens culinaris Modulate translocation /retention resulting in Mondal et al. (2019)
lowered toxicant levels in plant parts
Ni, Pb, Cd --------- Chick pea Increase proline content and decrease lipid Khan and Bano (2018)
peroxidation
Pb toxicity PBRB3 Mung bean Higher antioxidative enzyme activity Arif et al. (2019)
Pb toxicity CIK512 Radish Regulating the homeostasis of anti-oxidants Ahmad et al. (2018)
Osmotic stress ----------- Arabidopsis Higher proline production Chen et al. (2007)
tolerance
Heat stress ----------- Wheat Enhanced activity of antioxidant, proline Ashraf et al. (2019)
adenosine (iPA), izopentyl adenine (iP), and zeatin ribo- et al., 2014). Similarly, Bacillus spp. produce gibberellic
side (ZR) that promotes plant growth and shoot initiation acid (GA), which is associated with enhanced seed ger-
in associated plants (Poveda & González-Andrés, 2021). mination and stem elongation as reported in common
Z and ZR producing Bacillus spp. enhance the root exu- alder (Alnus glutinosa). GA-producing Bacillus spp. posi-
dation of amino acids in wheat which positively reshape tively correlated with increased macro-and micronutri-
the neighbouring soil microbial community (Kudoyarova ents, fructose, carotenoids and gamma- aminobutyric
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acid (Govindasamy et al., 2010; Nascimento et al., 2020). by Bacillus spp. induce the innate host immunity (Lee &
Furthermore, GAs produced by Bacillus spp. improved Kim, 2011). Lipopeptide-producing Bacillus strains form
the thermotolerance in wheat and soybean by inducing biofilms around plant roots thereby augmenting the an-
the expression of salicylic acid (SA) and jasmonic acid timicrobial activity in rhizosphere soil. Furthermore,
(JA) and downregulating ABA (Kang et al., 2019; Oleńska the lipopeptides produced by Bacillus have a plethora
et al., 2020). The multitude of phytohormones produced of beneficial applications in both industry and agroeco-
by B. subtilis and Bacillus spp. explain their positive effects system. In some cases, the lipopeptides can induce a
on the enhancement of plant growth and nutrient content negative effect on soil microbes. In addition, the VOCs
(Poveda & González-Andrés, 2021; Saxena et al., 2020). and phytohormones produced by B. subtilis might affect
endophytic and epiphytic microbiota. These beneficial
microbes which are a boon for the plant rhizospheric
Biocontrol and stimulation of immunity ecosystem may act as a curse for animal gut microbiota
when ingested. Bacillus subtilis forms its own ecosystem
The traditional method of disease triangle by plant path- through biofilm formation and produces several toxins to
ogens includes host susceptibility, pathogen virulence fight against pathogenic organisms. However, they may
and environmental conditions (Scholthof, 2007). Bacillus also affect the good microbes as they are trapped in its
spp. affect this disease triangle by direct and indirect ecosystem. There are a lot of hidden secrets in the plant
pathways (Radhakrishnan et al. (2017). The indirect rhizosphere that need to be explored in a timely man-
method includes the formation of biofilm, plant growth ner. A comprehensive understanding is required to avoid
promotion, competition for space and nutrients, and ISR. damage to plant and animal diversity.
In the direct method of disease control, B. subtilis produce In natural conditions, plants are exposed to a large range
various lipopeptides, cell lytic enzymes, antioxidants and of organisms like insects and micro-organisms (biotrophs,
hormones which affect a wide range of fungi and bacteria. hemi-biotrophs and necrotrophs). To cope with the ad-
Surfactin, iturin and fengycin are the major lipopeptides verse effects of pathogen infection, plants activate a layer
produced, which have a tremendous role in regulating a of defence apparatus depending upon the nature and life-
plethora of phytopathogens (Table 2). Surfactin is one of style of the pathogen (Nguyen et al., 2020). The ‘Molecular
the prominent lipopeptides produced by B. subtilis. It is a associated membrane repeats’ (MAMPS) along with the
cyclic lipoheptapeptide, consisting of three beta-hydroxy pattern-recognition receptors (PRRs) play a crucial role in
fatty acyl chains and seven amino acid residues (Wang recognizing the microbial molecules, thereby developing
et al., 2014). Surfactin shows antifungal activity against a particular defence response. The timing and type of im-
a wide range of fungal phytopathogens by inducing pore mune response characterize its nature, as the secondary
and ion channels through the lipid bilayer, cell cycle ar- ones are stronger as compared to the primary response.
rest and apoptosis. Fengycin is a cyclic lipodecapeptide Systemic acquired response (SAR) and ISR are likely to be
having 16–19 carbons of beta-hydroxy fatty acid, which the second defence responses in plants, mediated by dif-
upon changing its length and branching pattern pro- ferent phytopathogens (Figure 2). Once a pathogen infects
duces different isoforms (Ntushelo et al., 2019). It targets the plant, it reduces its energy metabolism and triggers
the phospholipase A2 enzyme and disrupts the fungi cell the defence mechanism for developing a long-lasting SAR.
wall. A higher concentration of fengycin ruptures the cell It has been shown that treatment of plant roots with cer-
membrane and forms permanent lesions affecting cellu- tain PGPB evolve such a protective effect on plants which
lar integrity. It elicits systemic resistance in plants and is can also protect the above-ground plant parts from a di-
effective against several genera of fungi. Iturins are am- verse scale of harmful microbes. This physiological state
phiphilic compounds having a heptapeptide backbone increases the defence capacity of plants simplified as ISR
and beta-hydroxy fatty acid chain of 17–19 carbon atoms. and the process is known as priming (Choudhary et al.,
Iturins target the fungi cells by ion pore mediating cell 2007). After getting the pathogen- related signal, these
wall disruption. They change the morphological struc- primed plants upregulate the generation of reactive oxygen
ture of conidia and affect hyphae formation in Fusarium species (ROS), defence-related gene expression, callose
spp. Bacillus subtilis produces many hydrolytic enzymes, deposition in the cell walls and collection of antimicro-
proteases, cellulase and glucanase, which reshape the bial phytoalexins (Nguyen et al., 2020). Pseudomonas spp.
rhizosphere environment so that it is more favourable for increase the basal defence mechanism of plants against
plant growth (Miljaković et al., 2020). Different Bacillus multiple soil pathogens by ISR (Romera et al., 2019). As
strains produce stable biofilms which act as a good bio- per recent reports, Bacillus spp. are in the front line of ISR
control agent against fungal pathogens. Similarly, ribo- induction while stimulating plant growth in a collective
somal peptide antibiotic such as bacteriocins secreted manner. It has been reported to protect plants against
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TABLE 2 Role of B. subtilis in plant disease control by lipopeptide production
S. No. Strains Host Pathogen Mechanism Reference

1. EA-CB0015 Chrysanthemum Botrytis cinera Iturin A Arroyave-Toro
C. acutatum Fengycin c et al. (2017)
2. 9407 Watermelon Acidovorax citrulli (Bacterial Surfactin reduces Fan et al. (2017)
fruit blotch) biofilm formation &
swarming motility
3. V26 Potato Fusarium oxysporum Surfactin Ben Khedher
Fusarium solani Fengycin et al. (2021)
Iturin
Bacillomycin
4. SL-6 Pome Alternaria alternata Surfactin Cozzolino
Botrytis cinera Iturin et al. (2020)
Fengycin
5. ATCC21556 Lettuce Fusarium oxysporum Iturin A Fujita and
Yokota (2019)
6. QST 713 Cucumber Powdery mildew Fengycin Punja et al. (2019)
Fusarium rot
7. ET-1 Lemon Green and gray mould Iturin A Ambrico &
Strawberry (P. digitatum; B. cinerea) Trupo, 2017
8. 9407 Apple Apple rot (Botryosphaeria Fengycin inhibits Fan et al. (2017)
dothidea) mycelial growth
9. NCD-2 Chinese cabbage Clubroot (Plasmidophora Fengycin Guo et al. (2019)
brassicae)
10. Q-11 Apple Blue mould (Penicillium Iturin Rodríguez-Chávez
expansum) Fengycin inhibits conidia et al. (2019)
germination
11. MBI 600 Cucumber Gray mould (Botrytis cinera) Fengycin Samaras
et al. (2021)
12. WL-2 Potato Potato late blight (Phytophthora Iturin (Oxidative stress, Wang et al. (2020)
infestans) cell wall disrupture)
13. NCD-2 Wheat Rhizoctonia solani AG-8 Surfactin Zhang et al. (2021)
Iturin
Fengycin
14. FZV-1 Pea Fusarium solani Surfactin Riaz et al. (2021)
Fengycin
Siderophores
15. GLB191 Grape Grapevine downy mildew Surfactin Li et al. (2019)
(oomycete Plasmopara Fengycin
viticola)
bacterial stem blight, crown rotting and leaf spotting It activates ABA and salicylic acid signalling pathways to
fungal pathogens, blue mould, nematodes and several restrict pathogen entry through stomata.
wilt-causing pathogens (Jinal & Amaresan, 2020). SAR is Bacterial lipopeptides can elicit ISR in bean mediated
phenotypically similar to ISR but the signalling pathways by surfactin and fengycin produced by B. subtilis S499
underlying it are different. SAR relies on the salicylic acid (Ongena et al., 2007). The same result was shown by
signalling pathway and accumulation of pathogenesis- B. subtilis CtpxS2-1 in Andean lupin (Yánez-Mendizábal
related proteins (PR genes) unlike ISR, which is elicited & Falconí, 2021). Other pieces of evidence show that bac-
by the ethylene/jasmonate signalling pathway and the terial VOCs such as 2,3-butanediol, induce ISR in plants
regulatory gene NPR1 (Dimopoulou et al., 2019). Abscisic through salicylic acid/ethylene signalling pathway and PR
acid (ABA) has been shown to play a key role in ISR in- gene upregulation (Farag et al., 2013). In some plants like
duction as ABA-deficient strains allowed stomatal closure tomato, B. subtilis CBR05 elicits the ISR response along
after treatment with B. subtilis FB17 (Kumar et al., 2012). with the biosynthesis of vitamin B in the de novo pathway
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(Chandrasekaran et al., 2019). Certain natural elicitors for biofilm production by secreting autoinducer signal-
such as 3,4-dihydroxy-3-methyl-2-pentanone are also ling molecules into the extracellular medium (Kalamara
responsible for ISR as observed in the case of the PGPR et al., 2018). ComQXPA proteins regulate the QS system
B. subtilis HN09, which dominates HN09-ISR (Liu et al., by phosphorylation and dephosphorylation. For instance,
2019). phosphorylation of ComA in the cytoplasm induces sur-
factin production.
Biofilm gives the microbes a sessile lifestyle from free
Biofilm production contributing to moving planktonic life where they can take several advan-
rhizocompetence tages like getting nutrition easily from root exudates and
surviving from environmental fluctuations. Shreds of ev-
Biofilms produced by microbes constitutes a mixture of idence suggest that citric acid of cucumber root exudates
species, it makes molecular genetic studies of a single spe- induce biofilm formation in Bacillus amyloliquefaciens
cies quite difficult (Arnaouteli et al., 2021). To overcome SQR9 and fumaric acid of banana root exudates had a
this difficulty, in vitro biofilm making is being carried out. significant role in chemotaxis and biofilm formation of B.
Bacillus subtilis biofilms are predominantly being used subtilis N11 (Zhang et al., 2014). These microbial biofilms
with the ancestral strain NCIB3610 and the three com- help the plants in different ways. Inoculation of biofilm-
monly used experimental systems are pellicle formation, forming PGPR like B. subtilis enhances crop yield through
where the complex bacteria form an interface between different plant growth mechanisms. Plant growth regula-
air and liquid, rugose colony formation where the bio- tors and antimicrobials produced by such PGPR regulate
film is formed on semisolid agar surfaces (Branda et al., the plant metabolic pathways in a positive way. Toxins
2001) and the formation of biofilm on plant roots using produced by B. subtilis such as YIT toxin through yitPOM
in vitro agricultural settings (Cairns et al., 2014). Time- operon act as a good competitor for other microbes serving
resolved analysis of B. subtilis pellicle biofilm formation as a biocontrol agent for the plant (Kobayashi & Ikemoto,
identified metabolic changes during the process like in- 2019). These can be used as good biofertilizers by inoc-
creasing the level of fatty acid degradation than biosyn- ulating with nitrogen-fixing microbes (Seneviratne et al.,
thesis, upregulation of iron metabolism, conversion from 2010). This biofilm formation in the root rhizosphere also
acetate to acetoin fermentation and enhanced Krebs cycle helps the plant in the management of its biotic and abi-
activity during the early phase (Pisithkul et al., 2019). otic stress balance. The biofilm-forming activity of B. am-
The metabolomic, transcriptomic and proteomic analy- yloliquefaciens has been shown to enhance the salt stress
ses has indicated that the complex metabolic remodelling tolerance of barley (Kasim et al., 2016). Several bacterial
of biofilm formation is highly regulated at the transcrip- metabolic pathways require biofilm formation for their
tional level. Bacillus subtilis uses quorum sensing (QS) optimal activity.
F I G U R E 2 Model of induced systemic resistance (ISR) and Systemic Acquired Resistance (SAR) mechanisms elicited by Bacillus subtilis
and pathogenic bacteria, respectively. SAR is phenotypically similar to ISR but the underlying signalling pathways are different. SAR relies
on the salicylic acid signalling pathway and accumulation of pathogenesis-related proteins unlike ISR, which is elicited by the ethylene/
jasmonic acid signalling pathway and regulatory gene NPR1. ISR is more diverse as compared to SAR
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Rhizosphere engineering and impact on beta indices signifying the presence of some new genera.
native plant endosphere and rhizosphere Those genera might be present in the soil at a very low
microbiomes density before, but they could not flourish due to some
environmental or genetic factors. The introduction of
Microbes are ubiquitously present in all soil ecosystems Bacillus may pave the path for their enrichment. Thus, the
and can be used as a strong weapon for establishing a bal- development of a modified bacterial community may af-
anced agricultural system (Köhl et al., 2019). Endophytic fect plants positively or negatively depending upon several
bacteria are the natural inhabitants of the plant, owing parameters. The interspecific competition varies accord-
to their growth and development benefits (Lastochkina ing to the geographical area, crop variety, and soil texture.
et al., 2020). Root endophytic communities are different Soil is the hotspot for all microbial communities. Its
from the rhizospheric community and they have a cru- management has a great impact on the overall microbi-
cial role in regulating plant metabolism. The invasion of ota. Bacillus subtilis produces both ribosomal and non-
exogenous species modifies it in a context-specific man- ribosomal peptides (NRP) as secondary metabolites, which
ner. A recent experiment using UniFrac measurement of has a great impact on indigenous microbes (Kiesewalter
beta diversity proved that inoculation of Bacillus species et al., 2020). The interactions of micro-organisms were
into the endophytic bacterial community has an impact evaluated by setting up a soil-derived semi-synthetic mock
on the evenness, diversity and composition (Gadhave community supplemented with NRP-deficient strain B.
et al., 2018). Due to interspecific competition, a reduc- subtilis WT P5_B1. 16S amplicon sequencings revealed
tion of Pseudomonas species occurred due to Bacillus that NRP-producing strains reduced the abundance of two
spp. All these experiments were conducted using high- genera of bacteria or had no impact on other microbial
throughput metagenome sequencing and assigning OTUs species. Engineering of Bacillus strains with no effect on
to each bacterial taxa. Inoculation of biofertilizer contain- endogenous microbiota would be beneficial for both plant
ing Bacillus sp. in sweet potato can increase the Shannon and soil ecosystems.
diversity index (H) by increasing the number of genera Plant roots associate with an enormous number of
(alpha- proteobacteria, flavobacteria) present before in- microbes that shape the plant's structural and func-
oculation (Figure 3; Salehin et al., 2020). In the soybean tional characteristics. The complex root microbial com-
root rhizobia where there is an abundance of alpha and munity is referred to as the second genome of the plant.
beta proteobacteria, invasion of other microbes has shown Thus, plant rhizosphere competence is a critical prereq-
to increase microbial diversity (Zhang et al., 2011). This uisite for the successful use of PGPR (Latif et al., 2020).
change in endophytic bacterial diversity has a correlation Rhizosphere–PGPR interactions vary with plants, seasons
with root nodule formation and is predicted to influence and the texture of the soil. Actinobacteria, Acidobacteria,
the soybean plant growth in a positive way. Proteobacteria, Chloroflexi, Bacteroidetes and Firmicutes
Rhizoremediation is an approach to deal with pol- are the abundant bacterial groups found in the rhizo-
luted environments in an eco-friendly manner (Alotaibi spheric soil. Inoculation of exogenous bacteria has shown
et al., 2021). Sometimes inoculation of endophytic bac- their up-and downregulation, influencing plant health.
teria with specific plants affects the endophytic bacterial Therefore, inoculation of PGPR should be done with a
community of the plant either positively or negatively. complete analysis of soil characteristics. Extensive re-
Inoculation of endophytic Bacillus cereus ERBP into search has been carried out to scrutinize the impact of
Euphorbia milii for formaldehyde removal can modify exogenous B. subtilis upon the rhizospheric microbial
the natural endophytic diversity (Khaksar et al., 2016). community. The invasion of Bacillus has a transient effect
Bacillus subtilis BSn5, an endophytic bacterium, isolated on the bacterial community, whereas a longer effect on
from Amorphophallus konjac, can evade the plant defense Eukaryota is shown in the tomato plant (Qiao et al., 2017).
response for its colonization. It produces a lantibiotic, sub- In the case of chamomile, there is a shift in microbial com-
tilomycin to bind with self-produced flagellin resulting in munity structure and beta indices, thereby adding new
endophytic colonization in Arabidopsis thaliana (Deng functionalities to plant metabolome (Schmidt et al., 2014).
et al., 2019). However, there was no quantitative difference in micro-
The application of Bacillus spp. as a plant inoculant bial communities. In some cases, the impact of the intro-
affects various attributes of the microbial community duction of Bacillus is soil specific that is the population
(Gadhave et al., 2018). As the endophytic bacterial com- density of Bacillus in clay soil had a significant negative
munity is a principal determinant of plant growth and correlation on bacterial diversity in cucumber rhizosphere
development, their change in nature and diversity could in comparison to loam and sandy soils (Li et al., 2016).
affect the beneficial bacteria and plant health. In general, Bacillus inoculation also increased the aerobic stability
the introduction of Bacillus spp. leads to an increase in the and fermentation quality of crops. However, it does not
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transfer genes horizontally to soil bacteria, which is a pos- Furthermore, these techniques can be used for finding
itive side attribute. new resources with new genetic makeup for transgenic
The introduction of B. subtilis to tobacco rhizospheric and hybrid plant technology (Parray & Shameem, 2020).
soil showed an opposite trend (You et al., 2014). Based on Metagenomics, meta-transcriptomics, meta-metabolomics
the construction of a 16S rRNA gene clone library and and meta-proteomics are the evolving technologies to un-
amplified ribosomal DNA restriction analysis (ARDRA), derstand the biological underpinnings of microbial com-
it was inferred that B. subtilis inoculation increased munities inoculated with B. subtilis. Integration of these
the numbers of γ-Proteobacteria and α-Proteobacteria technologies with bioinformatics and statistics will help
but reduced the numbers of bacterial groups such as β- to reveal the microbial correlation and functional machin-
Proteobacteria, Planctomycetes and Firmicutes (Table 3). ery (Ramakrishna et al., 2019). Rhizosphere engineering
Similarly, inoculation of B. subtilis Tpb55 in the tobacco based on the knowledge of signalling pathways would op-
rhizosphere decreased Actinobacteria level and increased timize plant health and production.
the abundance of Acidobacteria and Proteobacteria (Han Abiotic stress responses can be characterized by metab-
et al., 2016). Apart from the interaction among different olomics as the metabolomes of the plant and rhizospheric
bacterial groups, the inoculant can also affect the species microbiota change according to external stress responses.
richness of different microbial communities inhabiting These can be used to dissect the tripartite (plant-beneficial
the soil rhizosphere. The addition of B. amyloliquefaciens microbe [B. subtilis])- toxicogenic microbe) interaction
NJN-6 has been shown to decrease the alpha diversity of in agroindustrial research (Adeniji et al., 2020). Toxins
the fungal community (Yuan et al., 2017). Bacillus subti- generated by plant phytopathogens like Alternaria spp.,
lis 50-1 addition to Panax ginseng rhizosphere decreased Penicillium spp., Fusarium spp. have a negative impact on
the bacterial diversity and increased the fungal diversity plants. Metabolomic studies revealed catabolite repres-
(Dong et al., 2018). Thus, the microbial community inter- sion of poly-gamma-glutamic acid (PGA) produced by
action varies with the plant and microbial species compo- Bacillus licheniformis ATCC 9945, which has several appli-
sition of the rhizosphere. cations in food and cosmetics industry (Mitsunaga et al.,
2016). Furthermore, massive genetic mapping and data
analysis can provide a biochemical solution to molecular
Plant-microbe cross-signalling pathology. Genome sequencing and comparative analysis
of two B. subtilis strains, TR21 and R31 has shown several
Interaction between plant and B. subtilis is a complicated phytobeneficial characteristics like sporulation, antibiotic
interwoven system. The integration and fine-tuning of sig- synthesis, and quorum sensing for better rhizosphere engi-
nals produced by PGPR affect the local or distant plant neering (Li et al., 2021). Epigenomics can boost our knowl-
parts at the molecular and biochemical levels. To address edge and understanding of the below-ground dynamics
these interconnecting links, multi-omics approaches can through the study of methylation of DNA, alteration of
be used at genetic, proteomic, transcriptomic and me- histones and small non-coding RNAs. DNA methylation
tabolomic levels in plants (Figure 4; Meena et al., 2017). induced the expression of callose deposition and AtPR1
F I G U R E 3 Impact of exogenous
Bacillus spp. invasion on endophytic
microbiota. Inoculation of Bacillus spp.
increases the beta diversity index and
Shannon diversity index showing a
disbalance in species diversity. These
variations simultaneously affect the plant
physiological mechanisms positively
or negatively depending upon several
parameters
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gene in plants challenged with oomycetes pathogens iron homeostasis in Bacillus subtilis (Rizzi et al., 2019).
(Zogli & Libault, 2017). Similarly, epigenetic modifica- The use of biofilm-forming PGPR with novel scientific ap-
tion regulates the expression of NONEXPRESSOR OF proaches in agriculture would provide a big leap for the
PR GENES1 (NPR1/NIM1), a key player in SAR, thereby biofertilizer industry. Several studies have proved the ef-
conferring enhanced protection against pathogens (Singh fectiveness of PGPRs for plant growth promotion, phyto-
et al., 2014). Furthermore, chromatin assembly factor-1 hormone synthesis, nutrient uptake, systemic resistance
(CAF-1) modulates histone trimethylation of H3K4 and and abiotic stress (Ramakrishna et al., 2019; Ramakrishna
the expression of genes encoding PR5, PR1, WRKY53 et al., 2020). PGPB addition to marginal land helps in
and WRKY6 involved in defence responses against biotic the improvement of land productivity while influencing
stresses. The genome sequencing of B. amyloliquefaciens carbon cycling (Ramakrishna et al., 2020). However, if
FZB42 identified genes for the synthesis of secondary PGPRs act for their own existence and benefit, they are
metabolites associated with its survival in soil and com- likely to influence the existing microbiome of the plant. In
peting with neighbouring rhizospheric microbial com- close proximity, bacteria need to cooperate for nutrients
munity through the action of bacillibactin, lipopeptide and space while developing a dynamic communication
and polyketides (Chen et al., 2007). The inoculation with network like quorum sensing, quorum quenching and
Bacillus spp. altered the composition and abundance of production of several secondary metabolites (Mielich-
miRNA in Arabidopsis thaliana root (Xie et al., 2017). Süss & Lopez, 2015). The rhizospheric C:N ratio shapes
The differentially expressed miRNA (miR159b, miR400 the microbial diversity under different concentrations of
and miR8167a) enhance the expression of plant defence- atmospheric CO2. The availability of nitrogen and nutri-
related genes and polyamine biosynthesis genes associated ents favours the sequestration process along with plant
with root growth, fruit development and cell division. The growth (Grover et al., 2015). Different endospore-forming
small RNAs can be used in ‘cross-kingdom RNAi’ for gene Bacillus strains were characterized for suppressing plant
silencing in trans-position in host–microbe interaction to pathogens and stimulating plant growth and development.
control pathogenesis and crop production improvement Bacillus amyloliquefaciens FZB42 is successfully commer-
(Huang et al., 2019). cialized as a biofertilizer by ABiTEP GmbH. Similarly, it
was reported that biofertilizers comprising of charcoal
mixed B. subtilis and Azotobacter chroococcum entrapped
I M P ROV E M EN T OF SOIL QUALITY in organic matrix, cow dung rice bran, dried powder of
neem leaves and clay named as super granules of biofer-
Soil quality and fertility are defined by physical, chemical tilizers (SGBF) significantly improved wheat growth and
and biological properties of soil (Zhao et al., 2018). These yield (Kumar et al., 2015). Azospirillum, Bacillus megathe-
include soil organic carbon, pH, macro-and micronutri- rium var. Phosphoticum, Frateuria quaratia, Thiobacillus
ents required by plants, microbiota, soil enzymes, etc. thiooxidans and mycorrhiza combined with 100% dose of
recommended fertilizers treatment significantly improved
grain yield, nutrient content and biomass of the rice lan-
Biofertilizers drace Padmarekha (Nataraja et al., 2021).
Though there are several beneficial outcomes of using
Studies have been carried out for a better understanding B. subtilis and Bacillus spp. in the agroecosystem, cer-
of the plant growth potential of B. subtilis based on ge- tain limitations exist for their use as a biofertilizer. Due
nome sequencing, where strain EA-CB0575 increased the to the production quality, shelf life, competence in field
total dry weight (TDW) of tomato plants as compared to conditions and lesser efficiency as compared to chemical
non-inoculated plants in a greenhouse study, which was fertilizers, biofertilizers are not able to reach farmer’s satis-
associated with the presence of strain-specific genes and faction (Pathania et al., 2020). Lack of trained persons and
metabolic pathways (Franco-Sierra et al., 2020; Posada production facilities fail to produce quality and quantity
et al., 2018). It is crucial to understand the plant–microbe of required biofertilizers. Storage and transport play a key
interactions and root colonizing ability of the bacteria role in deciding the shelf life as their improper handling
before using it as a biofertilizer. A healthy plant–Bacillus decreases the microbial count resulting in inconsistent
relationship would be beneficial for the plant for sustain- field performance. Furthermore, environmental factors
able agriculture (Blake et al., 2021). Furthermore, zinc like temperature, rainfall, pH, soil erosion affect the field
nanoparticles constructed using B. subtilis enhanced conditions for optimal biofertilizer application (Schmidt
shoot length, root length and protein content in Zea & Gaudin, 2018). Chemical fertilizers show a fast response
mays (Sabir et al., 2020). Similarly, siderophore produc- to several stress conditions while PGPR association with
tion and biofilm formation are essential requirements for plant roots is time-consuming which makes the farmers
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TABLE 3 Impact of exogenous Bacillus sp. inoculation on rhizosphere microbial community
Bacillus sp. Plant Effect Reference

subtilis Brassica campestris Increased Proteobacteria and Actinobacteria Liu et al. (2018)
amyloliquefaciens NJN-6 In vitro study Decrease alpha diversity of fungal community Yuan et al. (2017)
subtilis 50-1 Panax ginseng Bacterial diversity decreased and fungal diversity Dong et al. (2018)
increased
subtilis Medicago sativa Bacterial diversity increased and transformation of Li et al. (2021)
microbial diversity composition
subtilis PTS-394 Tomato Longer impact on eukaryota than bacterial Qiao et al. (2017)
community
subtilis Co1-6 Chamomile Shifting of microbial community structure and Schmidt et al. (2014)
beta indices; added extra functionalities to plant
metabolism
subtilis B068150 Cucumber Clay soil—negative correlation with bacteria; No Li et al. (2016)
effect on loam and sandy soil
subtilis Tobacco γ-Proteobacteria and α-Proteobacteria increased; You et al. (2014)
β-Proteobacteria, Planctomycetes, and Firmicutes
decreased
subtilis Cotton Quantity and species richness of soil bacteria Lyu et al. (2019)
increased (mostly actinomycetes)
subtilis Tpb55 Tobacco Species enrichment; Actinobacteria levels decreased; Han et al. (2016)
Proteobacteria and Acidobacteria increased
-- Maize High bacterial diversity (Actinobacteria, Chaudhary et al. (2021)
Bacteroidetes, Acidobacteria, Chloroflexi)
bypass the use of biofertilizers. But, once the rhizospheric et al., 2021). The released nitrogen causes groundwater
interlink forms, it is long-lasting and can be extended to contamination and eutrophication of surface water. The
other crop plants. deposited form contributes to the global biodiversity loss
in the ecosystem and soil acidification. Substitution of
50% urea with B. subtilis biofertilizer can reduce the loss
Nitrogen cycling of nitrogen by 54%. The biofertilizer downregulates the
nitrogen-fixing nif H and amoA genes while upregulating
The growing food demand in the current world has medi- the denitrifying narG, nirS, nirK and nosZ genes in the soil
ated the farmers to use large amounts of chemical fertilizer (Sun et al., 2020b). The successful application of Bacillus
to increase the crop yield. The use of excessive nitrogen ferti- species in the purification of nitrogen- contaminated
lizer imposes a serious threat to the global soil nitrogen cycle. wastewater has been shown in several parts of the world
Between 1961 and 2007, nitrogen fertilizer intake and crop (Hlordzi et al., 2020). There are several methods of nitrate
yield increased, but the efficiency of nitrogen remained at removal like reverse osmosis, electrochemical reduction,
40% (Stevens, 2019). Increasing ammonia concentration in ion exchange and electrodialysis, which are expensive.
air leads to the formation of regional haze, blurred vision as The use of conventional methods like bioaugmentation
well as problems associated with respiratory and cardiovas- of wastewater with microbial agents in combination
cular systems. The use of B. subtilis as a biofertilizer reduced with the bioelectrochemical process speeds up denitri-
the percentage of ammonia emission by 44% (Sun et al., fication (Rahimi et al., 2020). This can be used for the
2020a). This bacterium downregulated the UreC gene ex- commercial production of butyrate from carbohydrate-
pression and upregulated several functional genes involved containing wastewater like dairy farm discharges. The
in ammonia oxidization. During composting manure, inoc- use of B. subtilis JD014 has been shown to be efficient in
ulation of B. subtilis with two other micro-organisms signifi- the removal of NO3-N and NO2-N along with a higher tol-
cantly reduced the ammonia nitrogen while increasing the erance for nitrogen toxicity (Yang et al., 2021). This also
nitrification process. This promotes composting technology helps in nitrogen fixation by purple non-sulphur bacte-
by reducing odour emissions. ria, Rhodopseudomonas palustris by nifH gene expression
Nitrogen loss from agricultural land occurs through and increasing oxygen uptake for nitrogenase activity
two pathways; leaching loss and nitrogen runoff (Mahmud (Arashida et al., 2019). Thus, B. subtilis biofertilizer could
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F I G U R E 4 Omics approaches to identify correlation among plant-microbe cross-talk, crop yield and soil fertility. It is essential to
understand the basic genetic makeup, DNA modifications, gene and protein expression patterns and metabolite dynamics for optimization
of plant growth and maintenance of soil microbiome
serve as a potent fertilizer for the microbial transforma- toxic metals. They have the potential to mobilize and im-
tion of nitrogen and reduce its loss from agroecosystems. mobilize the metals as well as decide their fate in differ-
In the modern era of technology, B. subtilis MTCC1455 ent geological forms. Bacillus subtilis has been shown as a
has been shown to be useful in the production of green cos- potent micro-organism in remediating soil contaminated
metics. Nitrate induces the production of surfactin which artificially with chromium (Li et al., 2019). It can be used
in combination with bioactive essential oils, form stable as a potent geomicrobiological stabilizer for immobiliza-
nanoemulsion, which can be stored for up to three months tion of Pb, Sb, Ni, Cu and Zn in alkaline soils. The applica-
(Ganesan & Rangarajan, 2021). Instead of using toxic prod- tion of nanohydroxyapatite (NHAP) along with B. subtilis
ucts which have several of side effects, the use of such green to cadmium contaminated soil improved soil remediation
cosmetics would be effective and beneficial for mankind. and increased rhizospheric community (Liu et al., 2018).
UV-mutated species B. subtilis 38, served as an efficient
sorbent of Hg, Cr, Cd and Pb (Wang et al., 2019). Certain
Bioremediation of pollutants species of B. subtilis (DBM) have been found to survive
in heavy metal contaminated soils, where DBM mineral
Industrialization and technological advances have led to a complexes were formed by phosphodiester bond forma-
world full of hazardous substances, toxic metals, organic tion thereby restricting the entry of heavy metals into the
and inorganic pollutants leaving a harmful impact on the bacterial cells as well as increasing its Cu and Pb sorption
ecosystem (Ferronato & Torretta, 2019). To purify the soil ability (Bai et al., 2019). The pH of the soil and the den-
from these toxic metals, steps have been taken by vari- sity of the bacteria in the soil community have a greater
ous governments (Wuana & Okieimen, 2011). However, impact on all these processes. Bacillus subtilis produce cy-
the use of several artificial substances and physiochemi- clic lipopeptide biosurfactants that can stabilize the pH,
cal processes has greater side effects on living organisms. salinity and temperature of the soil. These biosurfactants
Bioremediation is an effective eco- friendly technology are easily disposable, low toxic and can be prepared
to purify heavy metal contaminated soil, where bacte- from low-cost agricultural by-products. They can be ef-
ria play a vital role. Soil is the reservoir of microbes and ficiently used for remediating oil-contaminated soils due
they regulate the soil ecosystem by maintaining several to their excellent property of hydrocarbon emulsification
biogeochemical cycles of carbon, nitrogen and different (Nogueira Felix et al., 2019). Shreds of evidence suggest
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their effective role in the sorption of several heavy met- been used after removing ARGs and mobile genetic ele-
als in different types of soil textures (Selvam et al., 2021). ments (MGEs).
Bioelectrokinetic techniques have been used for the pu- Animal manure is used as compost for plant growth
rification of crude oil hydrocarbon, which is a combina- and development. Animal manure serves as a large repos-
tion of bioremediation and electrokinetic remediation. itory of ARGs due to the heavy use of antibiotics against
Bacillus subtilis AS2 used with this technique produces various animal pathogens (Zalewska et al., 2021). These
biosurfactants that increase the remediation efficiency by ARGs can enter the food chain via plant genomes. The
enhancing the total organic content, which is achieved by presence of ARGs on mobile genetic elements (MGEs)
the solubilization of hydrocarbons and faster electromi- allows the spreading of genes among the microbial com-
gration in the anodic compartment (Prakash et al., 2021). munity through horizontal gene transfer and transposons.
This method can be effectively used for the purification When they enter pathogenic bacteria, it is beneficial for
of petroleum contaminated soils and biosorption of heavy the bacteria but a threat to the host organism. The ad-
metals from an aqueous solution. Using this bacterium dition of B. subtilis (0.5%) in the livestock manure used
with planned biosorption techniques, underground water for composting can reduce the ARGs, MGEs and patho-
can be purified. Microbial biochar formulations (MBFs) genic bacteria by modulating pH (Duan et al., 2019). It
using biochar from microbial biowaste and B. subtilis SL- changed the absolute gene copy numbers of the ARGs
13 were used to treat potted pepper plants, which resulted while regulating their spreading ability. The use of mature
in enhanced plant growth as well as soil fertility improve- compost during swine manure composting decreased the
ment (Tao et al., 2019). relative abundance of ARGs, especially sulphanilamide
Even after the development of effective biofertilizers, ARGs and MGEs while promoting organic matter decom-
several farmlands use artificial or chemical fertilizers. As position. This is due to the rapid growth of Bacillus and
a result, the soil becomes contaminated with herbicides. Thermobacillus in the thermophilic period of composting
Some bacteria play an effective role in the biotransfor- and the reduction of bacterial hosts (Firmicutes) for ARG
mation of nicosulfuron herbicides in contaminated soils, and MGEs (ISCR1 and int1) (Wang et al., 2020).
without majorly affecting the rhizospheric microbial com- On the contrary, Bacillus sp. was reported to be the
munity (Zhang et al., 2020). Soil microbes play an import- major carrier of ARGs based on a study where a micro-
ant role in determining the diversity and composition of bial agent was used with pig manure for compost, which
plant communities while plants impact microbial species resulted in decreased levels of four categories of ARGs
richness, which regulates the plant metal uptake and its along with Firmicutes and Tn916/1545 while two cate-
utilization. gories increased their levels by amplification of intI1 and
several host bacteria (Cao et al., 2020). Although it is diffi-
cult to conclude whether B. subtilis acts as a bacterial host
Control of soil reservoirs of antibiotic for spreading ARGs or decreasing their abundance, by
resistance genes affecting other hosts, as it changes its nature in different
circumstances, we can infer that its positive or negative
Bacillus subtilis, the Gram-positive bacteria, has shown impact depends on the nature, chemical composition of
resistance against different antibiotics by several in- the manure, composting process and the concentration of
built physiochemical mechanisms. Recently, B. subtilis bacteria used in the process.
subsp. subtilis strain RK, with a novel class of amino-
glycoside transferase (AHP5), responsible for resistance
against aminoglycoside-based antibiotics has been iden- Carbon sequestration
tified (Parulekar et al., 2019). The cell wall transporters
present in bacteria are crucial for their resistance. The CO2 constitutes 76% of the total Greenhouse gas emission
BceAB type transporter present in B. subtilis is respon- and reducing its level in the atmosphere is one of the most
sible for resistance against cell wall active antimicrobial challenging issues faced by mankind (Rossi et al., 2016).
peptide, targeting the lipid II cycle of cell wall synthesis Biological systems play a crucial role in alleviating higher
(Kobras et al., 2020). This mechanism is often similar to CO2 concentration through carbon sequestration. Plants
the low GC content of Gram-positive microbes. Certain allocate about one-third of their photosynthetically fixed
mechanisms where the bacteria show resistance against carbon to soil (Jones et al., 2009). It is the largest reservoir
highly reactive oxidizing agents like chlorine dioxide of several minerals. The soil carbon sequestration is 3.5-5.2
and hydrogen peroxide are still elusive (Martin et al., Gt/year, which needs to be increased to mitigate the recent
2015). Although it harbours several resistance genes and issue of high CO2 levels leading to global warming (Duran
mechanisms, the positive traits of these bacteria have et al., 2021). The soil microbiota nourished by root exudates
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regulates the carbon efflux and influx pumps in the soil rhizo- applying as a biofertilizer. It can modulate the biogeochem-
sphere. The treatment of drylands with micro-organisms ical cycles, carbon sequestration process, and humus pro-
from biological crust increases the carbon adsorption capa- duction when applied at a higher concentration. The soil
bility of soil from 0.232 to 0.294 g/m2/day (Kheirfam, 2020). texture, composition, pH, temperature, climatic condition
Bacillus subtilis, a common PGPB used in the agricul- are some crucial factors that affect the bacteria association
tural sector has the potential for employment for carbon with plants and their efficiency. Before bacteria inocula-
sequestration in various growth conditions. Several ex- tion, the history of the farmland should be checked as the
periments have been carried out to check the carbon se- effect of Bacillus on the rhizospheric microbial community
questration ability of Bacillus. Carbonic anhydrase (CA) changes with the soil variety and texture. Some soil types
based enzymatic technology is an approach for carbon do not affect the microbiome while a different soil type de-
fixation and its biomitigation (Effendi & Ng, 2019). The creases the microbial diversity.
immobilized forms are efficient and can be used for in-
dustrial purposes. The CA isolated from B. subtilis VSG4
convert CO2 into CaCO3 in the immobilized form (Oviya CONC LUSION
et al., 2012). Bacillus sp. SS105, isolated from free-air CO2
enriched (FACE) condition, can transform CO2 to calcite Though there is a high demand for food production in
form due to the presence of beta-and gamma-carbonic the current scenario, a focus on sustainable agricultural
anhydrase genes. The CO2 sequestration efficiency and practices without harming the environment. PGPR, front-
calcite formation were observed by RUBISCO and CA en- benchers of the next- generation green revolution, are
zyme assays (Maheshwari et al., 2019). This sequestration good alternatives to chemical fertilizers. Bacillus subtilis
efficiency of bacteria also helps in the maintenance of sev- is one of the common PGPR to be used efficiently for op-
eral physiological and biological functions. The lipopep- timization of plant growth and yield. It protects the plant
tide type biosurfactants are also produced. Simultaneous from several stress conditions by ISR, biofilm formation,
carbon sequestration and biosurfactant production by lipopeptide, siderophore and exopolysaccharide secretion.
Bacillus would be beneficial from both commercial and It acts as an efficient denitrifying agent in the agroecosys-
agricultural points of view (Maheshwari et al., 2017). tem and maintains soil health by eco-friendly remediating
Gaseous CO2 and NaHCO3 are good alternatives to pro- technologies.
duce biosurfactants using Bacillus sp. ISTS2 (Sundaram &
Thakur, 2015).
Although the use of Bacillus spp. for carbon sequestra- Future perspectives
tion is an efficient method, it has some side effects with
reference to manure composting. The production of or- Future research should be focused on several antibiotic
ganic matter, humus or carbon conversion has a crucial resistance genes present in Bacillus whose transfer and
effect on plant growth and development. Bacillus subtilis interaction with other microbes and the effect on soil
applied at lower concentration (0.5%) reduced mineraliza- microbial diversity. Development of microbial consortia
tion in the cooling and maturity stages of composting and with B. subtilis for enhancement of crop yield without
enhanced the humification of carbon (Duan et al., 2020). any negative impact on the rhizosphere microbial com-
However, inoculation of B. subtilis at a higher percent- munity is the need of the hour. Targeting the endophytic
age (>2%) increased the fermentation process but inhib- microbiome of the seed, selecting plants compatible with
ited the synthesis of total organic carbon and humus (Lu the microbial inoculant or employing microbial engineer-
et al., 2021). Thus, the concentration of the bacteria used ing methods which ensure the continuity of beneficial mi-
for composting affects the sequestration ability of the soil. crobiota for generations are some options for the efficient
It is important to consider these factors while applying deployment of Bacillus subtilis and other PGPB for green
Bacillus as a biofertilizer. agriculture. Soil amendments and plant genome modifi-
Although B. subtilis is the common PGPR in use, there cation would help maintain soil quality. Metagenomics,
are some dark sides akin to Mr. Hyde character that need to meta-transcriptomics and epigenomics are several
be explored. It is the major carrier of antibiotic resistance emerging technologies that can be used for functional
genes and shows resistance against various pesticides. assessment of crop, soil and climatic factors for better in-
Though horizontal gene transfer has not been discovered tegration with the traditional system of agriculture. All
yet, it may affect the underground microbial diversity as these steps can enhance productivity and sustainability
it can activate several other transposons for gene transfer. in diverse agro-ecological conditions. Overall, the same
More research is required to gain a deeper insight into it. B. subtilis akin to the character of Dr. Jekyll and Mr. Hyde
The concentration of B. subtilis has to be considered while can have a positive or negative effect based on the density
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Cu(II) and Pb(II) adsorption. Journal Environmental Science,

of bacteria applied in the field, interactions with soil mi-
78, 328–337.
crobial community, soil characteristics, environment and Batool, T., Ali, S., Seleiman, M.F., Naveed, N.H., Ali, A., Ahmed, K.
plant species. The state-of-the-art research would help in et al. (2020) Plant growth promoting rhizobacteria alleviates
eliminating the negative attributes of Bacillus subtilis and drought stress in potato in response to suppressive oxidative
other PGPB on plant growth, soil health and environment. stress and antioxidant enzymes activities. Scientific Reports, 10,
16975. https://doi.org/10.1038/s41598-020-73489-z
CONFLICT OF INTEREST Ben Khedher, S., Mejdoub-Trabelsi, B. & Tounsi, S. (2021) Biological
potential of Bacillus subtilis V26 for the control of Fusarium
No conflict of interest to report for all authors.
wilt and tuber dry rot on potato caused by Fusarium species and
the promotion of plant growth. Biological Control, 152, 104444.
ORCID Blake, C., Christensen, M.N. & Kovács, Á.T. (2021) Molecular as-
Wusirika Ramakrishna https://orcid. pects of plant growth promotion and protection by Bacillus sub-
org/0000-0002-8571-5827 tilis. Molecular Plant Microbe Interactions, 34, 15–25. https://
doi.org/10.1094/MPMI-08-20-0225-CR
REFERENCES Branda, S.S., González-Pastor, J.E., Ben-Yehuda, S., Losick, R. &
Abdelshafy Mohamad, O.A., Ma, J.-B., Liu, Y.-H., Zhang, D., Hua, Kolter, R. (2001) Fruiting body formation by Bacillus subtilis.
S., Bhute, S. et al. (2020) Beneficial endophytic bacterial pop- Proceedings of the National Academy of Sciences of the United
ulations associated with medicinal plant Thymus vulgaris alle- States of America, 98, 11621–11626.
viate salt stress and confer resistance to Fusarium oxysporum. Cairns, L.S., Hobley, L. & Stanley-Wall, N.R. (2014) Biofilm forma-
Frontiers in Plant Science, 11, 47. tion by Bacillus subtilis: new insights into regulatory strategies
Adeniji, A.A., Babalola, O.O. & Loots, D.T. (2020) Metabolomic ap- and assembly mechanisms. Molecular Microbiology, 93, 587–
plications for understanding complex tripartite plant-microbes 598. https://doi.org/10.1111/mmi.12697
interactions: strategies and perspectives. Biotechnology Reports, Cao, R., Ben, W., Qiang, Z. & Zhang, J. (2020) Removal of antibiotic
25, e00425. resistance genes in pig manure composting influenced by inoc-
Ahmad, I., Akhtar, M.J., Mehmood, S., Akhter, K., Tahir, M., Saeed, ulation of compound microbial agents. Bioresource Technology,
M.F. et al. (2018) Combined application of compost and Bacillus 317, 123966. https://doi.org/10.1016/j.biortech.2020.123966
sp. CIK-512 ameliorated the lead toxicity in radish by regulat- Chandrasekaran, M., Paramasivan, M. & Chun, S.C. (2019) Bacillus sub-
ing the homeostasis of antioxidants and lead. Ecotoxicology tilis CBR05 induces Vitamin B6 biosynthesis in tomato through
Environmental Safety, 148, 805–812. the de novo pathway in contributing disease resistance against
Alotaibi, F., Hijri, M. & St-Arnaud, M. (2021) Overview of approaches Xanthomonas campestris pv. vesicatoria. Scientific Reports, 9, 6495.
to improve rhizoremediation of petroleum hydrocarbon- Chaudhary, P., Sharma, A., Chaudhary, A., Khati, P., Gangola, S. &
contaminated soils. Applied Microbiology, 1, 329–351. Maithani, D. (2021) Illumina based high throughput analysis
Ambrico, A. & Trupo, M. (2017) Efficacy of cell free supernatant from of microbial diversity of maize rhizosphere treated with nano-
Bacillus subtilis ET-1, an Iturin A producer strain, on biocontrol of compounds and Bacillus sp. Applied Soil Ecology, 159, 103836.
green and gray mold. Postharvest Biology and Technology, 134, 5–10. Chen, M., Wei, H., Cao, J., Liu, R., Wang, Y. & Zheng, C. (2007)
Arashida, H., Kugenuma, T., Watanabe, M. & Maeda, I. (2019) Expression of Bacillus subtilis proBA genes and reduction of
Nitrogen fixation in Rhodopseudomonas palustris co-cultured feedback inhibition of proline synthesis increases proline pro-
with Bacillus subtilis in the presence of air. Journal Bioscience duction and confers osmotolerance in transgenic Arabidopsis.
Bioengineering, 127(5), 589– 593. https://doi.org/10.1016/j. Journal Biochemistry Molecular Biology, 40, 396–403. https://
jbiosc.2018.10.010 doi.org/10.5483/bmbrep.2007.40.3.396.
Arif, M.S., Yasmeen, T., Shahzad, S.M., Riaz, M., Rizwan, M., Iqbal, Choudhary, D.K., Prakash, A. & Johri, B.N. (2007) Induced sys-
S. et al. (2019) Lead toxicity induced phytotoxic effects on mung temic resistance (ISR) in plants: mechanism of action. Indian
bean can be relegated by lead tolerant Bacillus subtilis (PbRB3). Journal Microbiology, 47, 289– 297. https://doi.org/10.1007/
Chemosphere, 234, 70–80. s12088-007-0054-2
Arnaouteli, S., Bamford, N.C., Stanley-Wall, N.R. & Kovács, Á.T. Cozzolino, M.E., Distel, J.S., García, P.A., Mascotti, M.L., Ayub, M.J.,
(2021) Bacillus subtilis biofilm formation and social interac- Benazzi, L.M. et al. (2020) Control of postharvest fungal patho-
tions. Nature Reviews Microbiology, 19, 600–614. https://doi. gens in pome fruits by lipopeptides from a Bacillus sp. Isolate
org/10.1038/s41579-021-00540-9 SL-6. Scientia Horticulturae, 261, 108957.
Arroyave- Toro, J.J., Mosquera, S. & Villegas- Escobar, V. (2017) Deng, Y., Chen, H., Li, C., Jianyi, X., Qi, Q. & Yuanyuan, X., et al.
Biocontrol activity of Bacillus subtilis EA-CB0015 cells and (2019) Endophyte Bacillus subtilis evade plant defense by pro-
lipopeptides against postharvest fungal pathogens. Biological ducing lantibiotic subtilomycin to mask self-produced flagellin.
Control, 114, 195–200. Communications Biology, 2,368, https://doi.org/10.1038/s4200
Ashraf, A., Bano, A. & Ali, S.A. (2019) Characterisation of plant 3-019-0614-0
growth-promoting rhizobacteria from rhizosphere soil of heat- Dimopoulou, A., Theologidis, I., Liebmann, B., Kalantidis, K.,
stressed and unstressed wheat and their use as bio-inoculant. Vassilakos, N. & Skandalis, N. (2019) Bacillus amyloliquefaciens
Plant Biology, 21, 762–769. MBI600 differentially induces tomato defense signaling path-
Bai, J., Chao, Y., Chen, Y., Wang, S. & Qiu, R. (2019) The effect of ways depending on plant part and dose of application. Scientific
interaction between Bacillus subtilis DBM and soil minerals on Reports, 9, 19120.
|
Dong, L., Xu, J., Zhang, L., Cheng, R., Wei, G., Su, H. et al. (2018) distachyon colonized by Bacillus subtilis B26. PLoS ONE, 10,
Rhizospheric microbial communities are driven by Panax e0130456.
ginseng at different growth stages and biocontrol bacteria al- Ganesan, N.G. & Rangarajan, V. (2021) A kinetics study on surfactin
leviates replanting mortality. Acta Pharmaceutica Sinica. B, 8, production from Bacillus subtilis MTCC 2415 for application
272–282. in green cosmetics. Biocatalysis and Agricultural Biotechnology,
Duan, M., Zhang, Y., Zhou, B., Qin, Z., Wu, J., Wang, Q. et al. (2020) 33, 102001.
Effects of Bacillus subtilis on carbon components and microbial Govindasamy, V., Senthilkumar, M., Magheshwaran, V., Kumar, U.,
functional metabolism during cow manure–straw composting. Bose, P., Sharma, V. et al. (2010) Bacillus and Paenibacillus spp.:
Bioresource Technology, 303, 122868. potential PGPR for sustainable agriculture. In: Plant growth
Duan, M., Zhang, Y., Zhou, B., Wang, Q., Gu, J., Liu, G. et al. (2019) and health promoting bacteria. Berlin, Heidelberg: Springer,
Changes in antibiotic resistance genes and mobile genetic ele- pp. 333–364.
ments during cattle manure composting after inoculation with Grover, M., Maheswari, M., Desai, S., Gopinath, K.A. &
Bacillus subtilis. Bioresource Technology, 292, 122011. Venkateswarlu, B. (2015) Elevated CO2: plant associated micro-
Duran, P., Mora, M., Matus, F., Barra, P.J., Jofré, I., Kuzyakov, Y. organisms and carbon sequestration. Applied Soil Ecology, 95,
et al. (2021) Biological crusts to increase soil carbon sequestra- 73–85.
tion: New challenges in a new environment. Biology, 10, 1190. Gowtham, H.G., Singh, B., Murali, M., Shilpa, N., Prasad, M.,
https://doi.org/10.3390/biology10111190 Aiyaz, M. et al. (2020) Induction of drought tolerance in to-
Effendi, S.S.W. & Ng, I.S. (2019) The prospective and potential of mato upon the application of ACC deaminase producing plant
carbonic anhydrase for carbon dioxide sequestration: a critical growth promoting rhizobacterium Bacillus subtilis Rhizo SF 48.
review. Process Biochemistry, 87, 55–65. Microbiological Research, 234, 126422.
El-Nahrawy, S., Elhawat, N. & Alshaal, T. (2019) Biochemical traits Guo, S., Zhang, J.W., Dong, L.H., Li, X., Asif, M., Guo, Q.G. et al.
of Bacillus subtilis MF497446: Its implications on the devel- (2019) Fengycin produced by Bacillus subtilis NCD-2 is involved
opment of cowpea under cadmium stress and ensuring food in suppression of clubroot on Chinese cabbage. Biological
safety. Ecotoxicology and Environmental Safety, 180, 384–395. Control, 136, 104001.
Fan, H., Ru, J., Zhang, Y., Wang, Q. & Li, Y. (2017) Fengycin pro- Han, Q.-Q., Lü, X.-P., Bai, J.-P., Qiao, Y., Paré, P.W., Wang, S.-M. et al.
duced by Bacillus subtilis 9407 plays a major role in the bio- (2014) Beneficial soil bacterium Bacillus subtilis (GB03) aug-
control of apple ring rot disease. Microbiological Research, ments salt tolerance of white clover. Frontiers in Plant Science,
199, 89–97. 5, 525.
Farag, M.A., Zhang, H. & Ryu, C.M. (2013) Dynamic chemical com- Han, T., Zhang, L., Gao, J., Kong, J., Feng, C., Wang, J. et al. (2016)
munication between plants and bacteria through airborne Correlation between root irrigation of Bacillus subtilis Tpb55
signals: induced resistance by bacterial volatiles. Journal of and variation of bacterial diversity in tobacco rhizosphere. Wei
Chemical Ecology, 39, 1007–1018. Sheng Wu Xue Bao =. Acta Microbiologica Sinica, 56, 835–845.
Ferronato, N. & Torretta, V. (2019) Waste mismanagement in de- Hashem, A., Abd Allah, E. F., Alqarawi, A. A., Al-Huqail, A. A., &
veloping countries: A review of global issues. International Shah, M. A. (2016). Induction of osmoregulation and modu-
Journal Environment Research Public Health, 16, 1060. lation of salt stress in Acacia gerrardii Benth. by arbuscular
Ferreira, C.M., Vilas-Boas, Â., Sousa, C.A., Soares, H.M. & Soares, mycorrhizal fungi and Bacillus subtilis (BERA 71). BioMed
E.V. (2019) Comparison of five bacterial strains producing Research International, 2016, 6294098.
siderophores with ability to chelate iron under alkaline condi- Hlordzi, V., Kuebutornye, F., Gyamfua, A., Abarike, E., Lu, Y., Chi,
tions. AMB Express, 9, 1–12. S. et al. (2020) The use of Bacillus species in maintenance of
Franco-Sierra, N.D., Posada, L.F., Santa-María, G., Romero-Tabarez, water quality in aquaculture: A review. Aquaculture Reports, 18,
M., Villegas-Escobar, V. & Álvarez, J.C. (2020) Bacillus subtilis 100503.
EA-CB0575 genome reveals clues for plant growth promotion Huang, C.Y., Wang, H., Hu, P., Hamby, R. & Jin, H. (2019) Small
and potential for sustainable agriculture. Functional Integrative RNAs–big players in plant-microbe interactions. Cell Host &
Genomics, 20, 575–589. Microbe, 26(2), 173–182.
Fujita, S. & Yokota, K. (2019) Disease suppression by the cyclic li- Jiang, C.H., Xie, Y.S., Zhu, K., Wang, N., Li, Z.J., Yu, G.J. et al. (2019)
popeptides iturin A and surfactin from Bacillus spp. against Volatile organic compounds emitted by Bacillus sp. JC03 pro-
Fusarium wilt of lettuce. Journal of General Plant Pathology, mote plant growth through the action of auxin and strigolac-
85, 44–48. tone. Plant Growth Regulation, 87, 317–328.
Gadhave, K.R., Devlin, P.F., Ebertz, A., Ross, A. & Gange, A.C. (2018) Jinal, N.H. & Amaresan, N. (2020) Evaluation of biocontrol Bacillus
Soil inoculation with Bacillus spp. modifies root endophytic species on plant growth promotion and systemic-induced re-
bacterial diversity, evenness, and community composition in a sistant potential against bacterial and fungal wilt- causing
context-specific manner. Microbial Ecology, 76, 741–750. pathogens. Archives Microbiology, 202, 1785–1794. https://doi.
Gagné-Bourque, F., Bertrand, A., Claessens, A., Aliferis, K.A. & org/10.1007/s00203-020-01891-2
Jabaji, S. (2016) Alleviation of drought stress and metabolic Jones, D.L., Nguyen, C. & Finlay, R.D. (2009) Carbon flow in the rhi-
changes in timothy (Phleum pratense L.) colonized with zosphere: carbon trading at the soil–root interface. Plant and
Bacillus subtilis B26. Frontiers. Plant Science, 7, 584. https://doi. Soil, 321, 5–33. https://doi.org/10.1007/s11104-009-992
org/10.3389/fpls.2016.00584 Kalamara, M., Spacapan, M., Mandic-Mulec, I. & Stanley-Wall, N.R.
Gagné-Bourque, F., Mayer, B.F., Charron, J.-B., Vali, H., Bertrand, (2018) Social behaviours by Bacillus subtilis: Quorum sensing,
A. & Jabaji, S. (2015) Accelerated growth rate and increased kin discrimination and beyond. Molecular Microbiology, 110,
drought stress resilience of the model grass Brachypodium 863–878.
|
Kang, S.M., Khan, A.L., Waqas, M., Asaf, S., Lee, K.E., Park, Y.G. subtilis modulates physiological responses of two different Triticum
et al. (2019) Integrated phytohormone production by the aestivum L. cultivars under drought stress. Plants, 9, 1810.
plant growth- promoting rhizobacterium Bacillus tequilensis Lastochkina, O., Pusenkova, L., Yuldashev, R., Babaev, M., Garipova,
SSB07 induced thermotolerance in soybean. Journal of Plant S., Blagova, D. et al. (2017) Effects of Bacillus subtilis on some
Interactions, 14, 416–423. physiological and biochemical parameters of Triticum aestivum
Kasim, W.A., Gaafar, R.M., Abou-Ali, R.M., Omar, M.N. & Hewait, L. (wheat) under salinity. Plant Physiology and Biochemistry,
H.M. (2016) Effect of biofilm forming plant growth promot- 121, 80–88.
ing rhizobacteria on salinity tolerance in barley. Annals of Lee, H. & Kim, H.Y. (2011) Lantibiotics, class I bacteriocins from
Agricultural Sciences, 61(2), 217–227. the genus Bacillus. Journal Microbiology Biotechnology, 21(3),
Khaksar, G., Treesubsuntorn, C. & Thiravetyan, P. (2016) Effect of 229–235.
endophytic Bacillus cereus ERBP inoculation into non-native Leontidou, K., Genitsaris, S., Papadopoulou, A., Kamou, N., Bosmali,
host: potentials and challenges for airborne formaldehyde re- I., Matsi, T. et al. (2020) Plant growth promoting rhizobacteria
moval. Plant Physiology and Biochemistry, 107, 326–336. isolated from halophytes and drought-tolerant plants: Genomic
Khan, N. & Bano, A. (2018) Effects of exogenously applied salicylic characterisation and exploration of phytobeneficial traits.
acid and putrescine alone and in combination with rhizobac- Scientific Reports, 10(1), 1–15.
teria on the phytoremediation of heavy metals and chickpea Li, L., Ma, J., Ibekwe, A.M., Wang, Q. & Yang, C.H. (2016) Cucumber
growth in sandy soil. International Journal of Phytoremediation, rhizosphere microbial community response to biocontrol agent
20, 405–414. Bacillus subtilis B068150. Agriculture, 6(1), 2.
Khan, N., Bano, A., Rahman, M.A., Guo, J., Kang, Z. & Babar, M.A. Li, Q., Xing, Y., Fu, X., Ji, L., Li, T., Wang, J. et al. (2021) Biochemical
(2019) Comparative physiological and metabolic analysis re- mechanisms of rhizospheric Bacillus subtilis-facilitated phyto-
veals a complex mechanism involved in drought tolerance in extraction by alfalfa under cadmium stress –Microbial diversity
Chickpea (Cicer arietinum L.) Induced by PGPR and PGRs. and metabolomics analyses. Ecotoxicology and Environmental
Scientific Reports, 9, 2097. Safety, 212, 112016.
Kheirfam, H. (2020) Increasing soil potential for carbon sequestra- Li, Y., Héloir, M.-C., Zhang, X., Geissler, M., Trouvelot, S., Jacquens,
tion using microbes from biological soil crusts. Journal of Arid L. et al. (2019) Surfactin and fengycin contribute to the protec-
Environments, 172, 104022. tion of a Bacillus subtilis strain against grape downy mildew
Kiesewalter, H.T., Lozano-Andrade, C.N., Strube, M.L. & Kovács, by both direct effect and defence stimulation. Molecular Plant
Á.T. (2020) Secondary metabolites of Bacillus subtilis im- Pathology, 20, 1037–1050.
pact the assembly of soil- derived semisynthetic bacterial Liu, N., Luo, X., Tian, Y., Lai, D., Zhang, L., Lin, F. et al. (2019)
communities. Beilstein Journal of Organic Chemistry, 16(1), The stereoisomeric Bacillus subtilis HN09 metabolite 3,
2983–2998. 4-dihydroxy-3-methyl-2-pentanone induces disease resistance
Kobayashi, K. & Ikemoto, Y. (2019) Biofilm-associated toxin and in Arabidopsis via different signalling pathways. BMC Plant
extracellular protease cooperatively suppress competitors in Biology, 19(1), 1–14.
Bacillus subtilis biofilms. PLoS Genetics, 15(10), e1008232. Liu, W., Zuo, Q., Zhao, C. Wang, S., Shi, Y. & Liang, S. et al. (2018)
Kobras, C.M., Piepenbreier, H., Emenegger, J., Sim, A., Fritz, Effects of Bacillus subtilis and nanohydroxyapatite on the metal
G. & Gebhard, S. (2020) BceAB-type antibiotic resistance accumulation and microbial diversity of rapeseed (Brassica
transporters appear to act by target protection of cell wall campestris L.) for the remediation of cadmium-contaminated
synthesis. Antimicrobial Agents and Chemotherapy, 64(3), soil. Environmental Science Pollution Research, 25, 25217–
e02241–e2319. 25226. https://doi.org/10.1007/s11356-018-2616-8
Köhl, J., Kolnaar, R. & Ravensberg, W.J. (2019) Mode of action of Lu, J., Wang, J., Gao, Q., Li, D., Chen, Z., Wei, Z. et al. (2021) Effect of
microbial biological control agents against plant diseases: microbial inoculation on carbon preservation during goat ma-
Relevance beyond efficacy. Frontiers Plant Sciences, 10, 845. nure aerobic composting. Molecules, 26, 4441.
Kudoyarova, G.R., Melentiev, A.I., Martynenko, E.V., Timergalina, Lyu, N., Shi, L., Liu, H.-Y., Si, A.-J., Li, Q.-S., Zhang, G.-L. et al. (2019)
L.N., Arkhipova, T.N., Shendel, G.V. et al. (2014) Cytokinin Effects of biological agent dripping on cotton Verticillium wilt
producing bacteria stimulate amino acid deposition by wheat and rhizosphere soil microorganism. Ying Yong Sheng Tai Xue
roots. Plant Physiology and Biochemistry, 83, 285–291. Bao = The. Journal of Applied Ecology, 30, 602–614.
Kumar, A.S., Lakshmanan, V., Caplan, J.L., Powell, D., Czymmek, Maheshwari, N., Kumar, M., Thakur, I.S. & Srivastava, S. (2017)
K.J., Levia, D.F. et al. (2012) Rhizobacteria Bacillus subti- Recycling of carbon dioxide by free air CO2 enriched (FACE)
lis restricts foliar pathogen entry through stomata. The Plant Bacillus sp. SS105 for enhanced production and optimization
Journal, 72(4), 694–706. of biosurfactant. Bioresource Technology, 242, 2–6.
Kumar, M., Bauddh, K., Sainger, M., Sainger, P.A. & Singh, R.P. Maheshwari, N., Kumar, M., Thakur, I.S. & Srivastava, S. (2019)
(2015) Increase in growth, productivity and nutritional status Cloning, expression and characterization of β-and γ-carbonic
of wheat (Triticum aestivum L.) and enrichment in soil micro- anhydrase from Bacillus sp. SS105 for biomimetic sequestration
bial population applied with biofertilizers entrapped with or- of CO2. International Journal of Biological Macromolecules, 131,
ganic matrix. Journal Plant Nutrition, 38, 260–276. 445–452.
Latif, S., Bibi, S., Kouser, R., Fatimah, H., Farooq, S., Naseer, S. et al. Mahmud, K., Panday, D., Mergoum, A. & Missaoui, A. (2021)
(2020) Characterization of bacterial community structure in the Nitrogen losses and potential mitigation strategies for a sustain-
rhizosphere of Triticum aestivum L. Genomics, 112, 4760–4768. able agroecosystem. Sustainability, 13, 2400.
Lastochkina, O., Garshina, D., Ivanov, S., Yuldashev, R., Khafizova, R., Martin, D.J., Wesgate, R.L., Denyer, S.P., McDonnell, G. & Maillard,
Allagulova, C. et al. (2020) Seed priming with endophytic Bacillus J.Y. (2015) Bacillus subtilis vegetative isolate surviving chlorine
|
dioxide exposure: an elusive mechanism of resistance. Journal B: Biointerfaces, 175, 256–263. https://doi.org/10.1016/j.colsu
of Applied Microbiology, 119(6), 1541–1551. rfb.2018.11.062
Medeiros, C.A.A. & Bettiol, W. (2021) Multifaceted intervention of Ntushelo, K., Ledwaba, L.K., Rauwane, M.E., Adebo, O.A. & Njobeh,
Bacillus spp. against salinity stress and Fusarium wilt in to- P.B. (2019) The mode of action of Bacillus species against
mato. Journal of Applied Microbiology, 131, 2387–2401. https:// Fusarium graminearum, tools for investigation, and future
doi.org/10.1111/jam.15095 prospects. Toxins, 11, 606.
Meena, K.K., Sorty, A.M., Bitla, U.M., Choudhary, K., Gupta, P., Oleńska, E., Małek, W., Wójcik, M., Swiecicka, I., Thijs, S. &
Pareek, A. et al. (2017) Abiotic stress responses and microbe- Vangronsveld, J. (2020) Beneficial features of plant growth-
mediated mitigation in plants: the omics strategies. Frontiers in promoting rhizobacteria for improving plant growth and health
Plant Science, 8, 172. in challenging conditions: A methodical review. Science of the
Mielich- Süss, B. & Lopez, D. (2015) Molecular mechanisms in- Total Environment, 743, 140682.
volved in Bacillus subtilis biofilm formation. Environmental Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B.
Microbiology, 17(3), 555–565. et al. (2007) Surfactin and fengycin lipopeptides of Bacillus
Miljaković, D., Marinković, J. & Balešević-Tubić, S. (2020) The sig- subtilis as elicitors of induced systemic resistance in plants.
nificance of Bacillus spp. in disease suppression and growth Environmental Microbiology, 9(4), 1084–1090.
promotion of field and vegetable crops. Microorganisms, 8(7), Oviya, M., Giri, S.S., Sukumaran, V. & Natarajan, P. (2012)
1037. Immobilization of carbonic anhydrase enzyme purified from
Mitsunaga, H., Meissner, L., Palmen, T., Bamba, T., Büchs, J. & Bacillus subtilis VSG-4 and its application as CO2 sequesterer.
Fukusaki, E. (2016) Metabolome analysis reveals the effect of Preparative Biochemistry and Biotechnology, 42(5), 462–475.
carbon catabolite control on the poly (γ-glutamic acid) biosyn- Parray, J.A. & Shameem, N. (2020) Chapter 3—molecular mechanism
thesis of Bacillus licheniformis ATCC 9945. Journal of Bioscience of plant-microbe interactions, sustainable agriculture. Academic
and Bioengineering, 121(4), 413–419. Press, 85–136, ISBN 9780128171097. /https://doi.org/10.1016/
Mondal, M., Biswas, J.K., Tsang, Y.F., Sarkar, B., Sarkar, D., Rai, M. B978-0-12-817109-7.00003-1
et al. (2019) A wastewater bacterium Bacillus sp. KUJM2 acts Parulekar, R.S., Barale, S.S. & Sonawane, K.D. (2019) Antibiotic re-
as an agent for remediation of potentially toxic elements and sistance and inhibition mechanism of novel aminoglycoside
promoter of plant (Lens culinaris) growth. Chemosphere, 232, phosphotransferase APH (5) from B. subtilis subsp. subtilis
439–452. strain RK. Brazilian Journal of Microbiology, 50(4), 887–898.
Naik, K., Mishra, S., Srichandan, H., Singh, P.K. & Sarangi, P.K. Pathania, P., Rajta, A., Singh, P.C. & Bhatia, R. (2020) Role of
(2019) Plant growth promoting microbes: potential link to plant growth- promoting bacteria in sustainable agriculture.
sustainable agriculture and environment. Biocatalysis and Biocatalysis and Agricultural Biotechnology, 30, 101842.
Agricultural Biotechnology, 21, 101326. Pisithkul, T., Schroeder, J.W., Trujillo, E.A., Yeesin, P., Stevenson,
Nascimento, F.X., Hernández, A.G., Glick, B.R. & Rossi, M.J. (2020) D.M., Chaiamarit, T. et al. (2019) Metabolic remodeling during
Plant growth-promoting activities and genomic analysis of the biofilm development of Bacillus subtilis. mBio, 10, e00623-19.
stress-resistant Bacillus megaterium STB1, a bacterium of ag- Posada, L.F., Álvarez, J.C., Romero-Tabarez, M., de-Bashan, L. &
ricultural and biotechnological interest. Biotechnology Reports, Villegas-Escobar, V. (2018) Enhanced molecular visualization
25, e00406. of root colonization and growth promotion by Bacillus subti-
Nataraja, T.H., Naika, R., Shankarappa, S.K., Reddy, K.V., lis EA- CB0575 in different growth systems. Microbiological
Abdelmohsen, S.A., Al-Harbi, F.F. et al. (2021) Productivity Research, 217, 69–80.
of paddies as influenced by varied rates of recommended nu- Poveda, J. & González-Andrés, F. (2021) Bacillus as a source of phy-
trients in conjunction with biofertilizers in local landraces. tohormones for use in agriculture. Applied Microbiology and
Agronomy, 11, 1165. Biotechnology, 105, 8629–8645.
Ndeddy Aka, R.J. & Babalola, O.O. (2016) Effect of bacterial inoc- Prakash, A.A., Prabhu, N.S., Rajasekar, A., Parthipan, P., AlSalhi,
ulation of strains of Pseudomonas aeruginosa, Alcaligenes fea- M.S., Devanesan, S. et al. (2021) Bio-electrokinetic remediation
calis and Bacillus subtilis on germination, growth and heavy of crude oil contaminated soil enhanced by bacterial biosurfac-
metal (Cd, Cr, and Ni) uptake of Brassica juncea. International tant. Journal of Hazardous Materials, 405, 124061.
Journal of Phytoremediation, 18, 200–209. Punja, Z.K., Tirajoh, A., Collyer, D. & Ni, L. (2019) Efficacy of Bacillus
Nguyen, N.H., Trotel- Aziz, P., Villaume, S., Rabenoelina, F., subtilis strain QST 713 (Rhapsody) against four major diseases
Schwarzenberg, A., Nguema-Ona, E. et al. (2020) Bacillus sub- of greenhouse cucumbers. Crop Protection, 124, 104845.
tilis and Pseudomonas fluorescens trigger common and distinct Qiao, J., Yu, X., Liang, X., Liu, Y., Borriss, R. & Liu, Y. (2017) Addition
systemic immune responses in Arabidopsis thaliana depending of plant-growth-promoting Bacillus subtilis PTS-394 on tomato
on the pathogen lifestyle. Vaccines, 8(3), 503. rhizosphere has no durable impact on composition of root mi-
Nicholson, W.L., Munakata, N., Horneck, G., Melosh, H.J. & Setlow, crobiome. BMC Microbiology, 17(1), 1–12.
P. (2000) Resistance of Bacillus endospores to extreme terres- Radhakrishnan, R., Hashem, A. & Allah, E.F.A. (2017) Bacillus: A
trial and extraterrestrial environments. Microbiology Molecular biological tool for crop improvement through bio-molecular
Biology Reviews, 64, 548–572. changes in adverse environments. Frontiers Physiology, 8, 667.
Nogueira Felix, A.K., Martins, J.J.L., Lima Almeida, J.G., Giro, Rahimi, S., Modin, O., Roshanzamir, F., Neissi, A., Alam, S.S.,
M.E.A., Cavalcante, K.F., Maciel Melo, V.M. et al. (2019) Seelbinder, B. et al. (2020) Coculturing Bacillus subtilis and
Purification and characterization of a biosurfactant produced wastewater microbial community in a bio-electrochemical sys-
by Bacillus subtilis in cashew apple juice and its application tem enhances denitrification and butyrate formation. Chemical
in the remediation of oil-contaminated soil. Colloids Surfaces Engineering Journal, 397, 125437.
|
Rajkumar, M., Ae, N., Prasad, M.N.V. & Freitas, H. (2010) Potential Schmidt, J. & Gaudin, A. (2018) What is the agronomic potential of
of siderophore-producing bacteria for improving heavy metal biofertilizers for maize? A meta-analysis. FEMS Microbiology
phytoextraction. Trends Biotechnology, 28(3), 142–149. Ecology, 94, fiy094. https://doi.org/10.1093/femsec/fiy094
Ramakrishna, W., Yadav, R. & Li, K. (2019) Plant growth promot- Schmidt, R., Köberl, M., Mostafa, A., Ramadan, E.M., Monschein,
ing bacteria in agriculture: Two sides of a coin. Applied Soil M., Jensen, K.B. et al. (2014) Effects of bacterial inoculants
Ecology, 138, 10–18. on the indigenous microbiome and secondary metabolites of
Ramakrishna, W., Rathore, P., Kumari, R. & Yadav, R. (2020) Brown chamomile plants. Frontiers Microbiology, 5, 64. https://doi.
gold of marginal soil: Plant growth promoting bacteria to over- org/10.3389/fmicb.2014.00064
come plant abiotic stress for agriculture, biofuels and carbon Schäfer, H. & Turgay, K. (2019) Spx, a versatile regulator of the
sequestration. Science of the Total Environment, 711, 135062. Bacillus subtilis stress response. Current Genetics, 65, 871–876.
Riaz, R., Khan, A., Khan, W.J., Jabeen, Z., Yasmin, H., Naz, R. https://doi.org/10.1007/s00294-019-00950-6
et al. (2021) Vegetable associated Bacillus spp. suppress the Schäfer, H., Beckert, B., Frese, C.K., Steinchen, W., Nuss, A.M.,
pea (Pisum sativum L.) root rot caused by Fusarium solani. Beckstette, M. et al. (2020) The alarmones (p) ppGpp are part
Biological Control, 158, 104610. of the heat shock response of Bacillus subtilis. PLoS Genetics,
Rismondo, J. & Schulz, L.M. (2021) Not Just Transporters: Alternative 16(3), e1008275.
functions of ABC transporters in Bacillus subtilis and Listeria Selvam, S., Jesuraja, K., Venkatramanan, S., Roy, P.D. & Kumari,
monocytogenes. Microorganisms, 9, 163. V.J. (2021) Hazardous microplastic characteristics and its role
Rizzi, A., Roy, S., Bellenger, J.P. & Beauregard, P.B. (2019) Iron as a vector of heavy metal in groundwater and surface water
homeostasis in Bacillus subtilis requires siderophore pro- of coastal south India. Journal of Hazardous Materials, 402,
duction and biofilm formation. Applied and Environmental 123786.
Microbiology, 85(3), e02439–e2518. Seneviratne, G., Weerasekara, M.L.M.A.W., Seneviratne, K.A.C.N.,
Rodríguez-Chávez, J.L., Juárez-Campusano, Y.S., Delgado, G. & Zavahir, J.S., Kecskés, M.L. & Kennedy, I.R. (2010) Importance
Pacheco Aguilar, J.R. (2019) Identification of lipopeptides of biofilm formation in plant growth promoting rhizobacterial
from Bacillus strain Q11 with ability to inhibit the germina- action. Plant growth and health promoting bacteria, pp 81–95.
tion of Penicillium expansum, the etiological agent of posthar- Berlin, Heidelberg: Springer.
vest blue mold disease. Postharvest Biology and Technology, Shah, A.A., Yasin, N.A., Akram, K., Ahmad, A., Khan, W.U., Akram,
155, 72–79. W. et al. (2021) Ameliorative role of Bacillus subtilis FBL-10
Romera, F.J., García, M.J., Lucena, C., Martínez- Medina, A., and silicon against lead induced stress in Solanum melongena.
Aparicio, M.A., Ramos, J. et al. (2019) Induced systemic re- Plant Physiology and Biochemistry, 158, 486–496.
sistance (ISR) and Fe deficiency responses in dicot plants. Singh, P., Yekondi, S., Chen, P.W., Tsai, C.H., Yu, C.W., Wu, K. et al.
Frontiers Plant Science, 10, 287. (2014) Environmental history modulates Arabidopsis pattern-
Rossi, S., Tubiello, F., Prosperi, P., Salvatore, M., Jacobs, H., triggered immunity in a HISTONE ACETYLTRANSFERASE1–
Biancalani, R. et al. (2016) FAOSTAT estimates of greenhouse dependent manner. The Plant Cell, 26, 2676–2688.
gas emissions from biomass and peat fires. Climatic Change, Soumare, A., Boubekri, K., Lyamlouli, K., Hafidi, M., Ouhdouch,
135, https://doi.org/10.1007/s10584-015-1584-y Y. & Kouisni, L. (2020) From isolation of phosphate solubi-
Sabir, S., Zahoor, M.A., Waseem, M., Siddique, M.H., Shafique, M., lizing microbes to their formulation and use as biofertilizers:
Imran, M. et al. (2020) Biosynthesis of ZnO nanoparticles using Status and needs. Frontiers Bioengineering Biotechnology, 7,
Bacillus subtilis: characterization and nutritive significance for 425.
promoting plant growth in Zea mays L. Dose-Response, 18(3), Stevens, C.J. (2019) Nitrogen in the environment. Science, 363(6427),
1559325820958911. 578–580.
Saikia, J., Sarma, R.K., Dhandia, R., Yadav, A., Bharali, R., Gupta, Sun, B., Bai, Z., Bao, L., Xue, L., Zhang, S., Wei, Y. et al. (2020a)
V.K. et al. (2018) Alleviation of drought stress in pulse crops Bacillus subtilis biofertilizer mitigating agricultural ammo-
with ACC deaminase producing rhizobacteria isolated from nia emission and shifting soil nitrogen cycling microbiomes.
acidic soil of Northeast India. Scientific Reports, 8, 3560. https:// Environment International, 144, 105989.
doi.org/10.1038/s41598-018-21921-w Sun, B.O., Gu, L., Bao, L., Zhang, S., Wei, Y., Bai, Z. et al. (2020b)
Salehin, A., Hafiz, M.H.R., Hayashi, S., Adachi, F. & Itoh, K. (2020) Application of biofertilizer containing Bacillus subtilis re-
Effects of the biofertilizer OYK (Bacillus sp.) inoculation on en- duced the nitrogen loss in agricultural soil. Soil Biology and
dophytic microbial community in sweet potato. Horticulturae, Biochemistry, 148, 107911.
6(4), 81. Sundaram, S. & Thakur, I.S. (2015) Biosurfactant production by
Samaras, A., Karaoglanidis, G.S. & Tzelepis, G. (2021) Insights into a CO2 sequestering Bacillus sp. strain ISTS2. Bioresource
the multitrophic interactions between the biocontrol agent Technology, 188, 247–250.
Bacillus subtilis MBI 600, the pathogen Botrytis cinerea and Tahir, H.A., Gu, Q., Wu, H., Raza, W., Hanif, A., Wu, L. et al. (2017)
their plant host. Microbiological Research, 248, 126752. Plant growth promotion by volatile organic compounds pro-
Saxena, A.K., Kumar, M., Chakdar, H., Anuroopa, N. & Bagyaraj, duced by Bacillus subtilis SYST2. Frontiers in Microbiology, 8,
D.J. (2020) Bacillus species in soil as a natural resource for plant 171.
health and nutrition. Journal of Applied Microbiology, 128, Tao, S., Wu, Z., Wei, M., Liu, X., He, Y. & Ye, B.C. (2019) Bacillus sub-
1583–1594. tilis SL-13 biochar formulation promotes pepper plant growth
Scholthof, K.B. (2007) The disease triangle: pathogens, the environ- and soil improvement. Canadian Journal of Microbiology,
ment and society. Nature Reviews Microbiology, 5, 152–156. 65(5), 333–342.
|
Upadhyay, S.K., Singh, J.S., Saxena, A.K. & Singh, D.P. (2012) Impact Andean lupin by lipopeptide production. Biotechnology Letters,
of PGPR inoculation on growth and antioxidant status of wheat 43(3), 719–728. https://doi.org/10.1007/s10529-020-03066-x
under saline conditions. Plant Biology, 14, 605–611. Zalewska, M., Błażejewska, A., Czapko, A. & Popowska, M. (2021)
US EPA. (1997). Attachment I -Final risk assessment of Bacillus Antibiotics and antibiotic resistance genes in animal manure
Subtilis. United States Environment Protection Agency report -Consequences of its application in agriculture. Frontiers
published in February 1997. Microbiology, 12, 610656.
Wang, T., Sun, H., Mao, H., Zhang, Y., Wang, C., Zhang, Z. et al. (2014) Zhang, N., Wang, D., Liu, Y., Li, S., Shen, Q. & Zhang, R. (2014)
The immobilization of heavy metals in soil by bioaugmentation Effects of different plant root exudates and their organic acid
of a UV-mutant Bacillus subtilis 38 assisted by NovoGro bio- components on chemotaxis, biofilm formation and coloni-
stimulation and changes of soil microbial community. Journal zation by beneficial rhizosphere-associated bacterial strains.
of Hazardous Materials, 278, 483–490. Plant and Soil, 374(1), 689–700.
Wang, X., Dong, G., Liu, X., Zhang, S., Li, C., Lu, X. et al. (2020) Zhang, Q., Stummer, B.E., Guo, Q., Zhang, W., Zhang, X., Zhang,
Poly-γ-
glutamic acid- producing bacteria reduced Cd uptake L. et al. (2021) Quantification of Pseudomonas protegens FD6
and effected the rhizosphere microbial communities of lettuce. and Bacillus subtilis NCD-2 in soil and the wheat rhizosphere
Journal of Hazardous Materials, 398, 123146. and suppression of root pathogenic Rhizoctonia solani AG-8.
Wang, X., Kong, Y., Zhao, H. & Yan, X. (2019) Dependence of the Biological Control, 154, 104504.
Bacillus subtilis biofilm expansion rate on phenotypes and the Zhang, Y.Z., Wang, E.T., Li, M., Li, Q.Q., Zhang, Y.M., Zhao, S.J. et al.
morphology under different growing conditions. Development, (2011) Effects of rhizobial inoculation, cropping systems and
Growth & Differentiation, 61(7–8), 431–443. growth stages on endophytic bacterial community of soybean
Wang, Y., Zhang, C., Liang, J., Wu, L., Gao, W. & Jiang, J. (2020) Iturin roots. Plant and Soil, 347(1), 147–161.
A extracted from Bacillus subtilis WL-2 affects Phytophthora in- Zhang, Z., Yang, D., Si, H., Wang, J., Parales, R.E. & Zhang, J. (2020)
festans via cell structure disruption, oxidative stress, and energy Biotransformation of the herbicide nicosulfuron residues in
supply dysfunction. Frontiers in Microbiology, 11, 2205. soil and seven sulfonylurea herbicides by Bacillus subtilis YB1:
Wuana, R.A. & Okieimen, F.E. (2011) Heavy metals in contaminated a climate chamber study. Environmental Pollution, 263, 114492.
soils: A review of sources, chemistry, risks and best available Zhao, Q., Tang, J., Li, Z., Yang, W. & Duan, Y. (2018) The influence
strategies for remediation. International Scholarly Research of soil physico-chemical properties and enzyme activities on
Notices, 2011, 402647. soil quality of saline-alkali agroecosystems in Western Jilin
Xie, S., Jiang, H., Xu, Z., Xu, Q. & Cheng, B. (2017) Small RNA pro- Province. China. Sustainability, 10, 1529.
filing reveals important roles for miRNAs in Arabidopsis re- Zhou, C., Zhu, L., Guo, J., Xiao, X., Ma, Z. & Wang, J. (2019) Bacillus
sponse to Bacillus velezensis FZB42. Gene, 629, 9–15. subtilis STU6 ameliorates iron deficiency in tomato by enhance-
Yadav, R., Ror, P., Rathore, P. & Ramakrishna, W. (2020) Bacteria ment of polyamine-mediated iron remobilization. Journal of
from native soil in combination with arbuscular mycorrhi- Agricultural and Food Chemistry, 67, 320–330.
zal fungi augment wheat yield and biofortification. Plant Zhu, Z., Zhang, H., Leng, J., Niu, H., Chen, X., Liu, D. et al. (2020)
Physiology Biochemistry, 150, 222–233. Isolation and characterization of plant growth-promoting rhizo-
Yadav, R., Ror, P., Rathore, P., Kumar, S. & Ramakrishna, W. (2021) bacteria and their effects on the growth of Medicago sativa L. under
Bacillus subtilis CP4, isolated from native soil in combination salinity conditions. Antonie Van Leeuwenhoek, 113, 1263–1278.
with arbuscular mycorrhizal fungi promotes biofortification, Zogli, P. & Libault, M. (2017) Plant response to biotic stress: Is there
yield and metabolite production in wheat under field condi- a common epigenetic response during plant-pathogenic and
tions. Journal Applied Microbiology, 131, 339–359. https://doi. symbiotic interactions? Plant Science, 263, 89–93.
org/10.1111/jam.14951 Zubair, M., Hanif, A., Farzand, A., Sheikh, T.M.M., Khan, A.R.,
Yang, T., Yang, Q., Shi, Y., Xin, Y., Zhang, L., Gu, Z. et al. (2021) Suleman, M. et al. (2019) Genetic screening and expression
Insight into the denitrification mechanism of Bacillus subtilis analysis of psychrophilic Bacillus sp. reveal their potential to
JD-014 and its application potential in bioremediation of nitro- alleviate cold stress and modulate phytohormones in wheat.
gen wastewater. Process Biochemistry, 103, 78–86. Microorganisms, 7, 337.
You, C., Zhang, L.M., Ji, S.G., Gao, J.M., Zhang, C.S. & Kong, F.Y.
(2014) Impact of biocontrol agent Bacillus subtilis on bacterial
communities in tobacco rhizospheric soil. Ying Yong Sheng Tai How to cite this article: Mahapatra, S., Yadav, R. &
Xue Bao, 25(11), 3323–3330. Ramakrishna, W. (2022) Bacillus subtilis impact on
Yuan, J., Zhao, M., Li, R., Huang, Q., Rensing, C. & Shen, Q. (2017) plant growth, soil health and environment: Dr. Jekyll
Lipopeptides produced by B. amyloliquefaciens NJN-6 altered the
and Mr. Hyde. Journal of Applied Microbiology, 132,
soil fungal community and non-ribosomal peptides genes harbor-
ing microbial community. Applied Soil Ecology, 117–118, 96–105.
3543–3562. Available from: https://doi.org/10.1111/
Yánez- Mendizábal, V. & Falconí, C.E. (2021) Bacillus subtilis jam.15480
CtpxS2-1 induces systemic resistance against anthracnose in

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Received: 30 December 2021

| Accepted: 4 February 2022

Bacillus subtilis impact on plant growth, soil health and

Subhasmita Mahapatra | Radheshyam Yadav | Wusirika Ramakrishna

Department of Biochemistry, Central Abstract

I N T RO DU CT ION (Ramakrishna et al., 2019). Continuous and indiscrimi-

TABLE 1 Bacillus subtilis mediated abiotic stress tolerance in plants

Abiotic stress Strain Plant Mechanism Reference

TABLE 2 Role of B. subtilis in plant disease control by lipopeptide production

S. No. Strains Host Pathogen Mechanism Reference

TABLE 3 Impact of exogenous Bacillus sp. inoculation on rhizosphere microbial community

Bacillus sp. Plant Effect Reference

Cu(II) and Pb(II) adsorption. Journal Environmental Science,

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