Plant Growth Promotion Using Bacillus cereus: Comparison
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Plant growth-promoting bacteria (PGPB) appear to be a sensible competitor to conventional fertilization, including mineral fertilizers and chemical plant protection products. Undoubtedly, one of the most interesting bacteria exhibiting plant-stimulating traits is, more widely known as a pathogen, Bacillus cereus. Several environmentally safe strains of B. cereus have been isolated and described, including B. cereus WSE01, MEN8, YL6, SA1, ALT1, ERBP, GGBSTD1, AK1, AR156, C1L, and T4S. These strains have been studied under growth chamber, greenhouse, and field conditions and have shown many significant traits, including indole-3-acetic acid (IAA) and aminocyclopropane-1-carboxylic acid (ACC) deaminase production or phosphate solubilization, which allows direct plant growth promotion. It includes an increase in biometrics traits, chemical element content (e.g., N, P, and K), and biologically active substances content or activity, e.g., antioxidant enzymes and total soluble sugar. Hence, B. cereus has supported the growth of plant species such as soybean, maize, rice, and wheat. Importantly, some B. cereus strains can also promote plant growth under abiotic stresses, including drought, salinity, and heavy metal pollution.

  • direct plant growth promotion
  • biocontrol
  • spore-forming bacteria

1. Biofilm Formation in Bacillus cereus

B. cereus strains colonize plant roots by forming biofilms [22][1]. Biofilm-forming microorganisms are beneficial to plant health due to increasing resistance to antibiotics, chemicals, heat, UV radiation, and other environmental stresses [23,24][2][3]. Some strains of B. cereus often merge with other bacterial species, resulting in the formation of mixed biofilms, e.g., two-species biofilms [25][4]. The B. cereus 905 strain isolated from the wheat rhizosphere can exhibit at least two modes of biofilm formation, depending on the environmental conditions. On one hand, B. cereus 905 is able to form floating biofilms (pellicles) in a similar way to Bacillus subtilis. However, this species can also form biofilm in a manner reminiscent of the biofilm formation using the pathogen Staphylococcus aureus [26][5].
Biofilm formation is associated with various gene expressions. Compared with B. subtilis, the regulatory mechanisms that are involved in biofilm formation in environmental B. cereus strains are not fully understood. However, recent scientific advances regarding this bacterial species provide more information about the genes and their functions associated with biofilm [27][6]. Studies conducted on the environmental isolates of B. cereus AR156, B. cereus 0–9, and B. cereus 905 show how biofilm formation is carried out [27,28][6][7].
In the environmental isolate B. cereus AR156, 23 genes associated with biofilm formation were identified by a random transposon insertion mutagenesis [28][7]. Importantly, the ClpYQ protease gene and genes involved in purine (purD and purH) and nucleotide biosynthesis—and GTP homeostasis—contribute to biofilm formation and swarm motility in B. cereus AR156. Furthermore, sigB and several other genes in the putative SigB regulon also play important roles in the biofilm formation in B. cereus AR156 [28][7]. It has also been shown that in B. cereus AR156, the comER gene plays an important role, regulating both biofilm formation and spore formation, and is likely to be a part of a regulatory pathway involved in the activation of Spo0A (the key regulator of biofilm formation and sporulation in B. cereus and B. subtilis). It has also been reported that the comER gene may regulate Spo0A activity through its effect on the small checkpoint protein Sda, which plays an important role in cell development processes in Bacillus spp. [29][8]. Another study has shown that the genes bcspo0A, bcsinI, and bcsinR, regulated by the Spo0A-SinI-SinR regulatory circuit, are essential for sporulation and biofilm formation in B. cereus AR156. Interestingly, bcspo0A and bcsinI genes are important for nematicidal activity and biocontrol against Meloidogyne incognita with B. cereus AR156 [30][9].
Importantly, the regulatory protein SpoVG derived from B. cereus 0–9 controls the activation of Spo0A transcription and is crucial for both sporulation and biofilm formation [31][10]. This has also shown that SpoVG influences AbrB and SinI/SinR networks and thus biofilm development. Moreover, the genes ptsI, sodA1, sodA2, gapB, and YmdB protein have been shown to play an important role in biofilm formation in B. cereus 0–9 [32,33,34,35][11][12][13][14]. Importantly, the above-mentioned studies show that the ptsI gene may be one of the key genes involved in the control of wheat sharp eyespot using B. cereus [32][11]. Moreover, the sodA1 gene has a crucial role in spore formation and tolerance to intracellular oxidative stress, while the sodA2 gene plays an important role in the negative regulation of phospholipase and hemolytic activity of B. cereus 0–9 [33][12]. The gapB gene, encoding glyceraldehyde-3-phosphate dehydrogenase (GAPDH), is involved in biofilm formation and extracellular DNA release of B. cereus 0–9 by regulating the expression or activity of the LrgAB autolysis regulator [34][13]. In turn, the YmdB protein is involved in the adaptation of B. cereus 0–9 to changing environmental conditions [35][14]. Interestingly, the sodA2 gene, encoding manganese-containing superoxide dismutase (MnSOD2), is particularly important in root colonization and biofilm formation in B. cereus 905 [36][15]. In the studies, Gao et al. [36,37,38][15][16][17], using random insertional mutagenesis of the TnYLB-1 transposon, identified the genes ptsI, ptsH, recA, hrcA, clc, feoB1, feoB2, ndk, and hutH, which regulate sodA2 expression in B. cereus 905, and are essential for biofilm formation.
In conclusion, B. cereus, compared with most species of the genus Bacillus, has a relatively well-studied mechanism of biofilm formation. Nevertheless, it is still necessary to search for the molecular mechanisms responsible for biofilm formation in order to gain potentially valuable information that could lead to an increase in the effectiveness of B. cereus as a PGPB, e.g., by overexpressing certain genes associated with biofilm formation in B. cereus.

2. Bacillus cereus as a Directly Plant Growth Stimulating Bacteria

The main mechanisms of PGPB activity are extensively covered by many review articles [9,39][18][19]; thereby, they are not discussed in detail. Instead, it focuses on the role of B. cereus strains as plant growth promoters. Due to their ubiquity and close interaction with plants, B. cereus strains are often considered as PGPB in various studies [40][20]. Frequently, a single B. cereus strain can promote the growth of many different plant species, indicating that it is well adapted to different habitat conditions. Plant growth stimulation using B. cereus strains is measured by parameters such as shoot/root length, fresh/dry biomass, and chlorophyll content. Stimulation of plant growth with B. cereus has been documented, e.g., for plants such as soybean (Glycine max L. Merr.), wheat (Triticum aestivum L.), Chinese cabbage (Brassica rapa L., Chinensis Group), maize (Zea mays), potato (Solanum tuberosum L.), pea (Pisum sativum L.), and rice (Oryza sativa L. var. FARO 44) [20,41,42,43,44][21][22][23][24][25].
Most of the studies on direct plant growth promotion with B. cereus have been conducted under controlled conditions. For instance, an experiment conducted in in vitro conditions showed that B. cereus MEN8 was capable of increasing seed germination parameters (e.g., vigor index, germination energy, or percentage of germination seeds) and stimulating plant growth parameters such as root and shoot length and plant weight of chickpea [45][26]. Another study in in vitro conditions reported that, after inoculation of rice seeds with B. cereus strain GGBSU-1, the germination percentage after 4 days was 100% compared with 65% in the control [44][25]. Furthermore, after 28 days, bacterial inoculation increased not only morphological parameters and biomass of rice seedlings, but also biochemical parameters, including chlorophyll a and b content, total soluble sugar, and α-amylase [44][25]. On the other hand, under greenhouse conditions, B. cereus T4S, isolated from the sunflower root endosphere by Adeleke et al. [46][27], promoted sunflower growth, including tap root length, root length, root number, root weight, seed weight, and shoot weight, in comparison with non-inoculated treatment. In addition, the study conducted under pot experiment by Kumar et al. [41][22] revealed the ability of B. cereus LPR2 (isolated from the spinach rhizosphere), alone and in combination with silver nanoparticles (AgNPs), to promote maize plant growth (including root and shoot growth and fresh and dry weight) through phosphate solubilization and IAA, HCN, and ammonia production. Moreover, maize seeds coated with the microbial inoculants B. cereus LPR2 and LPR2 with AgNPs exhibited a 37.5 and 25% larger increase in germination, respectively, compared with uninoculated seeds [41][22].
It was also observed that the application of B. cereus P8 resulted in a statistically significant increase in plant shoot and root biomass of pea plants under poly-house conditions [43][24]. This strain showed significant production of IAA and siderophores and had phosphate and potassium solubilization activity [43][24].
However, there were also studies carried out under field conditions. For instance, Ali et al. [42][23] showed that potassium solubilizing B. cereus was able to increase plant height and shoot dry weight, as well as increase the number of potatoes under field conditions. In addition, the application of this B. cereus strain contributed to an increase in total potato yield of approximately 20% compared with non-inoculated plants. Importantly, B. cereus also caused an increase in leaf N, P, and K concentrations in inoculated plants compared with the control [42][23]. In addition, B. cereus YL6 promoted soybean and wheat growth in pot experiments, including an increase in leaf total phosphorus [20][21]. Nevertheless, it also increased the yield of Chinese cabbage under field conditions. Its plant growth-promoting properties were related to IAA and gibberlines production and dissolution of inorganic and organic phosphorus [20][21].
However, despite the fact that B. cereus is capable of directly promoting plant growth (from biometric traits to NPK and chlorophyll content or enzyme activity), there is still little research under field conditions, which is an essential step in the commercialization of biofertilizers.

3. Plant Growth Promotion by Bacillus cereus in Combination with Other PGPB Species

As is well known, the application of one or more bacterial strains stimulating plant growth can be used as a more rational and safer alternative to agrochemicals [47][28]. To date, several studies have demonstrated the potential of bacterial consortia with B. cereus to improve plant growth. Nevertheless, not much further research is being conducted on the stimulation of plant growth with B. cereus in the consortium under controlled conditions. Interestingly, to date, research has shown that B. cereus with other bacterial strains (e.g., Pseudomonas spp. and Azospirillum spp.) can promote the growth of either crops or medicinal plants [48,49,50,51][29][30][31][32]. For instance, in studies on wheat in a 2-year experiment, the enhancement of plant growth treated in consortium with B. cereus (phosphorus-solubilizing microorganisms) has also been reported (under controlled and field conditions) [51][32]. The consortium containing B. cereus (accession no. LN714048) and Pseudomonas moraviensis (accession no. LN714047) led to an increase in biometric parameters, including plant height, plant fresh weight, and seeds weight [51][32]. Chauhan et al. [50][31], in a 180-day experiment under field conditions, showed a significant increase in plant biomass of turmeric (Curcuma longa L.) rhizomes by using a consortium of two bacterial strains: B. cereus TSH77 and B. endophyticus TSH42. Moreover, the study conducted by Sivasankariv and Anandharaj [48][29] on the Vigna unguiculata plant under in vivo and controlled conditions indicates that the consortium of B. cereus GGBSTD1 and Pseudomonas spp. GGBSTD3 (isolated from vermisources) acts as a potential biofertilizer due to its plant growth-promoting traits such as phosphate solubilization, IAA production, and siderophores. The results of the study showed that, compared with the control, the consortium significantly enhanced germination percentage, shoot length, root length, leaf area, chlorophyll a and b content in leaves, total chlorophyll content in leaves, fresh weight, and dry weight of plants. As far as chlorophyll is concerned, the positive effects of consortia involving B. cereus have already been reported in other studies. For instance, in a study conducted in a greenhouse, after double inoculation with a consortium of strains of B. cereus SrAM1 and Azospirillum brasilense, Stevia rebaudiana seedlings were characterized by an increase in chlorophyll a and chlorophyll b content and total chlorophyll content [49][30]. In addition, B. cereus in combination with other strains can also increase the activity of antioxidant enzymes, including catalase activity [49,51][30][32] and significant up-regulation of the ent-KO, UGT85 C, UGT74G1, and UGT76G1 genes responsible for steviol glycoside biosynthesis [49][30]. Interestingly, in the previously mentioned study by Chauhan et al. [50][31], a bacterial consortium with B. cereus increased the content of the main bioactive component, curcumin, by 13% compared with the control. In summary, B. cereus (in combination with other strains) not only promotes plants by increasing their yield and biometrics traits (root length, fresh weight, etc.), but also affects the activity of certain enzymes (e.g., antioxidant enzymes) and increases the concentration of biologically active substances that can be used in medicine, e.g., curcumin.

4. Bacillus cereus in the Alleviation of Abiotic Stress

Abiotic stress harms the biochemical, morphological, molecular, and physiological functioning of plants by exerting oxidative, osmotic, and ionic stresses. The most common ones are drought, salt, heavy metal pollution, and heat stress, to which crop plants are exposed worldwide [52,53][33][34]. Several experiments conducted by different researchers have shown that B. cereus strains are capable of promoting plant growth effectively not only in normal conditions but also in stressful environmental conditions [54,55,56,57][35][36][37][38]. In previous studies, it has been shown that, after inoculation, some plant growth-promoting B. cereus strains have considerably beneficial effects on both physiological (dry and fresh weight, shoot and root length, germination) and biochemical traits (chlorophyll content, relative water content, protein, proline, and antioxidant activity) under abiotic stress conditions. Abiotic stress tolerance induced with B. cereus strains in plants is mediated by mechanisms such as phytohormone and ACC deaminase activity, antioxidant defense (SOD, POD, APX, CAT, GR), accumulation of osmolytes, volatile compounds (VOCs), and heavy metals bioremediation, including exopolysaccharide production (EPS) and alteration of root morphology [56,58,59,60,61,62][37][39][40][41][42][43].
Recently, in the context of climate change, it has been particularly important to find PGPB effective in mitigating drought and heat stresses. Under drought stress conditions (greenhouse experiment), B. cereus UFGRB2 affected the photosynthetic efficiency in soybean by sustaining the potential quantum yield of PSII and maintaining the photosynthesis rate, while a decrease was observed in non-inoculated plants [63][44]. In another case, the application of B. cereus MKA4 under wheat (drought-sensitive variety HD2733) drought stress resulted in a noticeable increase in SOD, catalase, and glutathione reductase (GR) activities compared with control plants under drought conditions (pot experiment) [61][42]. In addition, co-inoculation of wheat under drought stress (under field conditions) using B. cereus (accession CP003187.1) with Pseudomonas fluorescens (accession GU198110.1) led to a significant increase in chlorophyll content and improved yield parameters compared to the control [64][45].
Interestingly, the ACC deaminase-producing B. cereus KTES strain was able to enhance shoot and root length, shoot and root weight, and leaf area of Solanum lycopersicum under heat stress conditions in the growth chamber [56][37]. Moreover, isolated by Khan et al. [53][34], the endophytic strain B. cereus SA1 was able to produce IAA, gibberellin, and organic acids. Inoculation of this bacterial strain improved the values of biomass, chlorophyll content, and chlorophyll fluorescence of soybean under standard and heat stress conditions after 10 days of cultivation in the growth chamber (controlled conditions). B. cereus SA1 also reduced the levels of heat-stress-produced abscisic acid (ABA) and reduced the amount of salicylic acid (SA).
Importantly, strains of B. cereus are also able to enhance plant growth promotion under saline conditions. For instance, isolated from the Cenchrus ciliaris (halophytic weed) endophytic strain, B. cereus (accession LN714048) caused a significant increase in proline, phytohormones, antioxidant enzymes, and yield parameters such as seed weight and spike length of wheat under saline stress (in vitro conditions) [65][46]. Interestingly, Zhou et al. [66][47] have shown that B. cereus, through enhancing the activity of antioxidants, increases the growth and photosynthesis ability of cucumber seedlings grown on a solid medium irrigated with 150 mM NaCl solution. On the other hand, Wang et al. [67][48] conducted a more comprehensive study (pot experiment) focusing on elucidating the mechanisms of action of B. cereus in the mitigation of salinity stress in Glycyrrhiza uralensis. For instance, B. cereus G2 noticeably enhanced proline and glycine betaine content due to upregulated expression of the BADH1 gene and soluble sugar content due to the activated expression of α-glucosidase and SS genes, which may lead to a reduction in the osmotic potential of the cell, thereby mitigating osmotic stress. In addition, B. cereus G2 mitigated oxidative stress through the effect of antioxidant enzymes [67][48].
B. cereus strains are also capable of mitigating plant stress caused by heavy metals, including arsenic, nickel, bo r, cadm, chromium, lead, copper, and zinc [60,68,69,70,71][41][49][50][51][52]. Under cadmium stress conditions (pot experiment), B. cereus S6D1-105 was able to promote the growth of rice under hydroponic conditions. Cd-tolerant B. cereus had the ability to, for example, solubilize potassium and phosphate and produce siderophores, thereby increasing plant biomass, chlorophyll content, and antioxidant enzyme activities, including polyphenol oxidase, catalase, superoxide dismutase, and ascorbate peroxidase and reducing malondialdehyde in either rice leaves or roots [68][49]. Similar patterns were also obtained by other authors, e.g., Sahile et al. [69][50] documented that B. cereus ALT1 reduces ABA and enhances SA contents in soybean plants under Cd stress conditions (growth chamber conditions). In addition, after plant inoculation of B. cereus ALT1, the researchers noted an increase in yield parameters and chlorophyll content. Additionally, B. cereus can also alleviate plant stress caused by the presence of chromium in the soil [70][51]. Application of B. cereus contributed to direct Brassica nigra plant growth promotion, including increasing shoot and root length and biomass, compared with the uninoculated control. Moreover, inoculation with this strain reduced chromium toxicity (pot experiments, greenhouse). Importantly, after B. cereus application, the photosynthetic pigments content was enhanced as well as increases in chlorophyll a, chlorophyll b, and carotenoids were observed. In addition, the strain contributed to an increase in the activity of antioxidant enzymes such as superoxide dismutase, catalase, and peroxidase [70][51].
Research has also demonstrated the possibility of alleviating plant stress caused by heavy metals by combining B. cereus with other bacterial strains. For example, the consortium of three heavy metal-tolerant plant growth-promoting bacteria—B. cereus MG257494.1, Alcaligenes faecalis MG966440.1, and Alcaligenes faecalis MG257493.1—showed tolerance to cadmium, lead, copper, and zinc (in vitro conditions) [71][52]. The results of the greenhouse study showed that the inoculation resulted in reduced bioaccumulation of heavy metals in the roots and shoots of Sorghum vulgare L.
In conclusion, using some B. cereus strains can effectively mitigate the damage caused by abiotic stresses primarily through IAA and ACC deaminase production, increasing antioxidant activity, proline content, and bioremediation of heavy metals.
Tested strains that stimulate plant growth under adverse environmental conditions, such as B. cereus (accession CP003187.1), B. cereus KTES, B. cereus SA1, B. cereus (accession LN714048), B. cereus G2, B. cereus S6D1-105, and B. cereus ALT1 alone or in combination with other PGPBs, can be considered for use in developing biofertilizers.

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