Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress (2024)

3.1. Mechanism of action of microbial biocontrol agents

B. subtilis is a gram-positive bacterium that forms biofilms on inert surfaces and possesses many transcriptional factors (Stanley et al., 2003). Different strains of B. subtilis synthesize a variety of hydrolytic enzymes, including i.e. cellulases, proteases, and β‐glucanases. Cazorla et al. (2007) suggested that since B. subtilis has the ability to secrete antibiotics and hydrolytic enzymes, it can modify its’ environment in a self-beneficial manner and also produce resistant endospores to sustain itself under adverse conditions. The ability of B. subtilis to exhibit biocontrol activity is dependent upon three factors: (1). host vulnerability; (2). pathogen virulence; and (3). the environment. Potential biocontrol mechanisms of B. subtilis are presented in Fig. 1. Importantly, any molecular changes (changes in gene expression) can directly or indirectly influence the mechanisms illustrated in Fig. 1. Additionally, genetically engineered enhancement of B. subtilis with known biocontrol traits may interact with existing mechanisms in a synergistic manner (Dotaniya et al., 2016).

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Fig. 1

Mechanisms of Bacillus subtilis in biological control of biotic stress.

Bacteria also produce the cell-wall-degrading enzymes and various metabolites that can limit the growth or activity of other microorganisms (Shoda, 2000). Notably, B. subtilis strains are known to synthesize antibiotic lipopeptides, including fengycin, surfactin, and iturin. Lipopeptides are low molecular weight compounds with amphiphilic features. Surfactants and antimicrobial compounds produced by B. subtilis are receiving more attention. Lipopeptide genes occur in many species and strains of biocontrol agents and some with enhanced capacity to produce antibiotics and limit fungal root pathogens have been commercialized (Joshi and McSpadden Gardener, 2006). Romero et al. (2007) reported that lipopeptides provide protection to plants under both pre- and post-harvest conditions by directly suppressing pathogenic fungi or by inducing systemic resistance in host plants. B. subtilis strains PCL1608 and PCL1612 produce a high level of antibiotics, especially iturin A which serves as the principal mechanism underlying the control of Fusarium oxysporum and Rosellinia necatrix (Cazorla et al., 2007). These results are supported by previous reports indicating that iturin A exhibits antifungal activity against a variety of target fungi (Chitarra et al., 2003). A recent study reported that B. amyloliquefaciens L-1 was a good biocontrol agent against pear ring rot (Pingping et al., 2017). Bacillus strain 6051 exhibits strong, very stable biofilm formation and also produces surfactin, indicating that it would a good biocontrol agent against pathogenic bacteria (Bais et al., 2004). As previously mentioned, the lipopeptides produced by B. subtilis represent diverse antifungal and anti-bacterial antibiotics including fengycins, iturins and, surfactins (Mnif and Ghribi, 2015). Meena and Kanwar (2015) reported that while surfactants have strong antibacterial activity, they do not have an impact on fungi.

Iturins are categorized into A, C, D, and E iturins; mycosubtilin; D, F, and L bacillomycins; and bacillopeptin (Mnif and Ghribi, 2015). Iturins exhibit antimicrobial activity against fungi and yeast and are considered as an excellent biopesticide (Wang et al., 2015). Fengycins, a type of plipastatin, and A, B, or C fengycin (Wang et al., 2015) are less hemolytic than surfactins and iturins but have strong antifungal activity and limit the growth of bacteria and fungi (Ongena and Jacques, 2008). B. subtilis also produces peptide antibiotics called bacteriocins that play an important role in innate host immunity. Bacteriocins are grouped into four classes based on their genetic and biochemical properties. Class 1 bacteriocins, called lantibiotics, are commonly used as an antibiotic (Joseph et al., 2013). Lantibiotics synthesized by B. subtilis are categorized into A and B types based on their antimicrobial activity and chemical structure (Kumar et al., 2012).

The biocontrol activity exhibited by B. subtilis can also be attributed to indirect mechanisms. B. subtilis is a common soil microbe but is present freely except in soils where it has been applied in high doses. Evidence also indicates that B. subtilis occurs as an endophyte of plant roots (Fall et al., 2004). Indirect mechanisms associated with the biocontrol activity of B. subtilis against plant pathogens include, biofilm formation, plant growth promotion (PGP), competition for nutrients and colonization sites, ability to induce cell lysis, and induced systemic resistance (ISR) (Wang et al., 2018). Antibiotic substances play an important role in disease control by microbes, including B. subtilis. More than 24 antibiotic substances have been reported to be produced by B. subtilis. The produced substances include peptides, proteins, and non-peptides based substances. Non-peptide antibiotics can be categorized as ribosomal and non-ribosomal peptide antibiotics (Wang et al., 2015). B. subtilis also forms biofilms on plant roots which help to produced lipopeptides and augment their antimicrobial activity in the soil (Davey et al., 2003).

In summary, many strains of Bacillus subtilis exhibit the ability to act as biocontrol agents against pathogenic fungi and thus can be used to suppress disease. Several mechanisms, both direct and indirect, are responsible for their ability to control pathogenic fungi. These include the production of a wide array of antibiotic compounds (lipopeptides), the ability to form endospores, the ability to form biofilms on root surfaces, and the ability to induce host systemic host resistance, and stimulate plant growth. In this regard, biofilm development is more vigorous in wild strains of B. subtilis than in laboratory or commercial strains (Kinsinger et al., 2003).

3.2. Induction of host resistance and plant growth

B. subtilis is a species of PGPR that are known to activate plant host defense response (host resistance) against pathogens. Host cells undergo ultrastructural and cytochemical changes in response to a pathogen attack. B. subtilis is known to activate induced systemic resistance (ISR) in the hosts that they occupy, which increases host resistance to plant pathogens. The activation of ISR by B. subtilis is known to induce the synthesis of jasmonic acid (JA), ethylene, and the NPR1-regulatory gene in plants (Garcia-Gutierrez et al., 2013).

These defense responses are systemically activated at distances far-removed from the original site of disease and confer a level of disease resistance against viruses, fungi and bacteria throughout the plant. The activation of ISR is associated with cell wall degradation, de novo protein production of glucanases and chitinases, and the production of phytoalexins linked to disease resistance. The application of B. subtilis strain (AUBS1) increases host production of phenylalanine ammonialyase (PAL), peroxidase (POD), and de novo protein synthesis in rice leaves (Jayaraj et al., 2004). Another study reported that B. subtilis strain (UMAF6614) induced the secretion of SA and JA defense-related responses in melons; making the plants more resistant to powdery mildew (Garcia-Gutierrez et al., 2013). Bacillus subtilis also enhances the synthesis of enzymes and PR proteins in host tissues in tobacco, resulting in increased resistance to mosaic virus, as evidenced by the reduced level of mosaic symptoms observed in plants treated with B. subtilis than in non-treated plants (Lian et al., 2011). Host enzymes that are induced by B. subtilis include peroxidase, (POD), polyphenol oxidase (PPO), and superoxide dismutase (SOD), as well as various hormones, whose increased synthesis results in ISR against early and late blight in tomato seedlings (Chowdappa et al., 2013). Bacillus subtilis strain (Sb4-23) mediates ISR in plant hosts through indirect, rather than direct mechanisms (Wang et al., 2018). The use of another strain of Bacillus subtilis strain reduced root-knot nematodes activity in tomato plants by activating ISR (Adam et al., 2014). The enhancement of plant growth is often linked with ISR. Bacillus subtilis (BS21-1) has been demonstrated to be an excellent biocontrol agent and has been reported to decrease disease incidence in four vegetable crops through ISR (Lee et al., 2014). In summary, B. subtilis has been shown to activate ISR in many plant crops, leading to increased disease resistance as evidenced by a lower number of pathogenic infections. It is an abundant and genetically diverse organism that has been used to produce numerous commercial biocontrol products. The application of a Bacillus strain activates ISR and promotes plant growth. Further studies should be conducted on Bacillus to identify new strains that can be used address many different plant diseases, while at the same time, acting as a PGPR and making host plants more stress tolerant.

3.3. Synergistic interactions between B. subtilis and root nodule bacteria

Inoculation of plant roots with rhizobia may result in a smaller number of nodules produced when a new strain is used. New strains may not be able to compete with indigenous strains. The root nodulation process is based on an exchange of signals between the host and bacterium which leads to the establishment of the rhizobia in host tissues, nodulation, and the promotion of plant growth through enhanced uptake of nutrients from the surrounding soil (Tilak et al., 2006). A positive effect on plant disease control and growth has been observed when plants have been exposed to both root nodule bacteria and B. subtilis. Microbes that are associated with roots, including free living, endophytic, rhizospheric, and symbiotic, can induce the synthesis of phytohormones in their plant hosts or in some cases produce the hormones directly (Sgroy et al., 2009). Zaidi et al. (2009) reported that B. subtilis is directly involved in P solubilization and exhibits a synergism with arbuscular mycorrhizal fungi (Kohler et al., 2007).

Various genera of bacteria have been isolated from the soil and rhizosphere, including Bacillus, Acinetobacter, Enterobacter, Pseudomonas, and Sinorhizobium (Sorty et al., 2016). Another study revealed that Bacillus, Enterobacter, Arthrobacter, Mycobacterium, Cellulosimicrobium, and Pseudomonas were all associated with soybean roots (Egamberdieva et al., 2016). While the application of a PGPR did not adversely affect the rhizobacterial strain that was present, inoculation with P. putida and Pseudomonas fluorescens or a Bacillus strain had a positive effect on root nodulation, enzyme production, and plant growth relative to non-inoculated plants (Tilak et al., 2006). Endophytic diazotrophic bacteria have been reported to synthesize plant growth hormones (JA, GA3, IAA, and ABA) in roots of the halophyte shrub, Prosopis strombulifera (Piccoli et al., 2011). In another study, the production of IAA by Pseudomonas and Ochrobactrum, was confirmed in bacteria when subjected to adverse environmental conditions (Mishra et al., 2017). Großkinsky et al. (2016) reported that the Bacillus species, B. megaterium, B. cereus, and B. subtilis, produced cytokinins. Arbuscular mycorrhizal (AM) fungi together with Bacillus subtilis were applied to geranium with results indicating that AM fungi alone increased yield by 49.4%; and when AM fungi were combined with B. subtilis, yield increased by 59.5%. Although oil content did not increase on a dry weight basis, total oil yield was increased significantly due to greater biomass production (Alam et al., 2011). In summary, B. subtilis exhibit a synergistic effect on plant growth when they are applied in combination with AM fungi. The combined application results in greater promotion of plant growth, increased production of enzymes, antioxidants, P solubilization, biocontrol activity, root nodulation, and nitrogen fixation. The evidence indicates that a greater effort should be made to develop a commercial formulation of PGPR strains of Bacillus spp.; especially those that readily form endospores.

3.4. Induction of a systemic agent in plant roots

As previously discussed, soil contains many diverse microorganisms with the potential of beneficial antagonistic properties. Utilization of select microbes, such as B. subtilis, can result in increased plant growth and the suppression of plant pathogens. This is accomplished through the production of many defense-related compounds in plant host tissues that lead to ISR, by direct antibiosis through the synthesis of diverse antimicrobial substances by the beneficial microbes; as well the direct synthesis of plant hormones and other beneficial compounds by the beneficial microbes. Roots strongly bind soil particles and are readily colonized by microorganism (Barea et al., 2005). Bacteria compete for nutrients with other resident microbes and with plant roots. As a result, the interactions between rhizosphere microbes and plants are critical. Mutual beneficial interactions have evolved, such as the provision of carbon compounds to resident microbes by their plant hosts, and increased nutrient and water uptake for the plant host due to the activity of the beneficial microbes. Induction of ISR and enhanced plant growth are other benefits derived by plants through their interactions with microbes (Gouda et al., 2018). Among microbes, B. subtilis plays a significant role in PGPR activity and biocontrol. Activation of ISR is one of the benefits obtained from the use of B. subtilis. The ISR stimulus could be salicylic acid (De Meyer and Hofte, 1997) and/or the presence of rhizobacteria (Hallmann et al., 1999). Bacillus subtilis can be used to induce resistance (Aliye et al., 2008) by inducing the synthesis of defense enzymes in the host, such as POD, PPO, and PAL. Plants activate defense mechanisms when a pathogen attack is perceived. This defense response often leads to systemic acquired resistance (SAR) process and the induction of a hypersensitive reaction; resulting in the formation of brown, desiccated tissue (Ryals et al., 1996). Disease severity is limited when the defense signal transduction pathway is activated (Van Wees et al., 2000). Inoculation of plants with B. subtilis strain (pf4) resulted in a high level of SAR. In relative comparison to non-inoculated plants, much higher levels of germination (96.5%), shoot length (9.0 cm), root length (8.03 cm), and vigor index (1703) were for inoculated plants (Anand et al., 2010). Seed treatment with Pseudomonas fluorescens I and II enhanced root biomass production in sunflower (Bhatia et al., 2005). Similar results were obtained in Castor seeds inoculated with P. fluorescence and B. subtilis, with greater increases in growth obtained with P. fluorescence than with B. subtilis (Khanuchiya et al., 2012). When tomato seeds were treated with Bacillus subtilis (EPC016), a significant increase in seedling growth was observed relative to non-inoculated plants (Ramyabharathi et al., 2013).

3.5. Alleviation of biotic stress in plants by Bacillus subtilis

Members of genus Bacillus can survive as endospores for long periods of time under harsh environmental conditions. They can also secrete a variety of secondary metabolites that stimulate plants to grow and increase disease resistance. A few studies have been conducted to examine the physiological processes that increase stress tolerance in plants in response to the presence of Bacillus species (Radhakrishnan et al., 2017). Organic farming practices consider the application of bacterial agents as an eco-friendly and safe way to increase productivity and disease resistance in crops (Dihazi et al., 2012). Myresiostis et al. (2015) have stated that the utilization of B. subtilis can reduce use of synthetic pesticides and insecticides in modern agriculture. Chemical fungicides and insecticides have a negative impact on beneficial soil microbes present that help to increase plant growth. Thus, the use of beneficial bacteria, such as. B. subtilis, could augment the application of other microbial pesticides as the use of chemical pesticides are terminated (Girolami et al., 2009). Bacillus thuringiensis (Bt), and the use of Bt toxin, provide a broad range of insecticide control (Navon, 2002), Bt also inhibits the growth of insect larvae and increases plant growth (Arrizubieta et al., 2016). B. cereus, B. amyloliquefaciens, and B. subtilis are also used to control pests (Gadhave et al., 2016). PGPR, such as B. subtilis, P. fluorescens, P. putida, and Paenibacillus administered through the use of coated, aluminum, gold, or silver nanoparticles, not only increased plant growth but also limited fungal growth in the rhizosphere. Therefore, the concept of nano-biofertilizers should be considered. Encapsulated nano-biofertilizers have been reported to deliver fertilizer to target cells, thus dramatically reducing the amount of fertilizer needed and preventing pollution through runoff (Mishra and Kumar, 2009). Herbicides such as pendimethalin and metalochlor, used in conjunction with polymers, such as polystyrene sulphonate and polyallylamine hydrochloride, have also been used in an encapsulated form for the sustained release of active ingredient to a specific place; thereby greatly improving the efficiency and safety of weed control (Kanimozhi and Chinnamuthu, 2012).

Peer review under responsibility of King Saud University.

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