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Review

Potential of Bacillus halotolerans in Mitigating Biotic and Abiotic Stresses: A Comprehensive Review

by
Pelias Rafanomezantsoa
*,
Abbas El-Hasan
* and
Ralf Thomas Voegele
Department of Phytopathology, Institute of Phytomedicine (360), Faculty of Agricultural Sciences, University of Hohenheim, Otto-Sander-Str. 5, 70599 Stuttgart, Germany
*
Authors to whom correspondence should be addressed.
Stresses 2025, 5(2), 24; https://doi.org/10.3390/stresses5020024
Submission received: 27 January 2025 / Revised: 17 March 2025 / Accepted: 21 March 2025 / Published: 25 March 2025
(This article belongs to the Collection Feature Papers in Plant and Photoautotrophic Stresses)
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Abstract

:
Bacillus halotolerans, a halophilic bacterial species of the genus Bacillus, is emerging as a biological control agent with immense potential for sustainable agriculture, particularly in extreme conditions and environmental rehabilitation. This review summarizes the current state of research on B. halotolerans, emphasizing its diverse applications in the biocontrol of plant pathogens, plant growth promotion under salinity stress, nematode management, and bioremediation. B. halotolerans utilizes several mechanisms such as the production of siderophores and phytohormones, secretion of exopolysaccharides, and the release of antifungal and nematicidal compounds, which allows it to mitigate both abiotic and biotic stresses in various crops, including wheat, rice, date palm, tomato, and others. In addition, genomic and metabolomic analyses have revealed its potential for secondary metabolite production that improves its antagonistic and growth-promoting traits. Despite significant progress, challenges remain in translating laboratory results into field applications. Future research should focus on formulating effective bioinoculants and field trials to maximize the practical utility of B. halotolerans for sustainable agriculture and environmental resilience.

1. Introduction

The increasing global demand for food security, coupled with the detrimental environmental effects of chemical plant protection products (cPPPs), has necessitated a shift toward more sustainable agricultural practices. While effective for controlling phytopathogens and enhancing yields, the widespread dependence of chemical inputs has resulted in severe ecological consequences, including soil and water pollution, harm to non-target organisms, and the development of resistant pathogens [1,2,3,4]. Public concerns about chemical residues in products have led to stricter regulations on cPPP usage, encouraging the exploration of biological alternatives. Biocontrol, a crucial component of integrated pest management (IPM) systems, represents a promising solution for reducing the negative impacts of phytopathogens while promoting sustainable and safe agricultural practices [5,6]. This approach includes the use of beneficial microorganisms such as Bacillus spp., known for their capacity to protect plants through competition and antagonism, to mitigate crop losses and improve yields, particularly in protected and organic vegetable production systems [7].
Among plant growth-promoting bacteria (PGPB), Bacillus species stand out due to their ability to colonize plant tissues endophytically without causing harm, offering a dual advantage in plant protection and growth promotion [8]. The genus includes a wide range of species such as B. amyloliquefaciens, B. subtilis, B. velezensis, B. pumilus, and B. siamensis, each recognized for their capabilities to produce enzymes, induce systemic resistance in plants, and synthesize antimicrobial metabolites [9]. These bacteria have also been extensively utilized in the production of commercial biocontrol products, such as Serenade® and Rizhovital®, which are highly effective against foliar, soil-borne, and post-harvest pathogens [10]. The production of robust endospores by this Gram-positive bacterium further enhances their advantages over other bacterial biocontrol agents (e.g., Pseudomonas spp.), allowing for efficient production, extended shelf-life, and easier formulation [11,12].
Members of Bacillus are known by the release of an extensive arsenal of antimicrobial peptides, including iturin, fengycin, bacillomycin, and surfactin, which exhibit broad-spectrum biocidal activity against pathogens while inducing systemic resistance in plants [13,14,15,16]. Additionally, Bacillus species produce a variety of volatile and non-volatile compounds that synergistically combat phytopathogens [17]. These capabilities, coupled with the ability to activate plant defense enzymes such as peroxidase (POX), polyphenol oxidase (PPO), and phenylalanine ammonia-lyase (PAL), make Bacillus a cornerstone of modern biocontrol strategies [18,19].
Due to its unique physiological and ecological attributes, B. halotolerans has emerged as a particularly promising candidate for sustainable agriculture within this genus. This species is well-adapted to extreme environmental conditions, such as high salinity and drought, which are increasingly common in agricultural soils, particularly in arid and semi-arid regions [20]. B. halotolerans has demonstrated impressive biocontrol capabilities, producing a wide range of secondary metabolites, including antifungal lipopeptides, volatile organic compounds, and antioxidant enzymes that protect plants from both biotic and abiotic stresses [21,22,23]. Furthermore, its ability to enhance plant growth under stressful conditions has been observed in various crops, including wheat, tomatoes, and potatoes, making it a valuable tool in enhancing agricultural resilience and productivity [21,23,24,25,26]. This article presents a comprehensive review of the potential of B. halotolerans as a biocontrol agent in sustainable agriculture. It consolidates current research to showcase the physiological, biochemical, and molecular characteristics that make B. halotolerans uniquely suited for mitigating plant diseases and enhancing growth under stressful environmental conditions. The review also explores the diverse habitats of B. halotolerans, its ability to produce antimicrobial metabolites, and its role in alleviating abiotic stresses, such as salinity and drought. Furthermore, the article emphasizes the importance of this species in IPM strategies and its potential to reduce dependency on cPPPs while ensuring crop productivity and environmental sustainability.

2. Morphological, Biochemical and Molecular Characteristics of B. halotolerans

B. halotolerans is a gram-positive, rod-shaped bacterium known for its adaptability to diverse and often extreme environmental conditions [27]. This species, previously classified as Brevibacterium halotolerans, has been reclassified through advanced molecular and biochemical tools, solidifying its position within the genus Bacillus [28]. It is an alkaliphilic organism capable of thriving in saline soils, which underpins its classification as a halotolerant species. Its historical classification and recent re-evaluation reflect ongoing efforts to establish its taxonomy, with strains like DSM 8802 and MS50-18A serving as references for its biochemical and genetic characterization [28,29].
Strains of B. halotolerans exhibit distinct morphological and biochemical profiles depending on their habitat and isolation source. On LB medium, colonies appear smooth and creamy with regular edges [30], or they may be milky white, opaque, and wrinkled [31]. On TSA medium, the bacterium forms smooth, glossy light-brown colonies [27]. The rod-shaped cells are approximately 0.84–1.49 μm × 2.08–4.10 μm (width × length) and motile with peritrichous flagella. Endospores from this strain are commonly observed after seven days of incubation, highlighting their robustness in adverse conditions [27].
Biochemically, B. halotolerans displays a wide range of metabolic capabilities. It grows on diverse carbon sources, including glucose, cellulose, sucrose, lactose, fructose, and maltose [31]. It demonstrates remarkable salt tolerance, with some strains capable of thriving in a medium supplemented with a 1.5M NaCl [32]. Notably, the KKD1 strain has been shown to grow at 13% salinity in previous studies [23]. B. halotolerans exhibits impressive environmental adaptability and plant-growth-promoting traits. It can grow at temperatures ranging from 4 to 45 °C, with optimal growth at 30 °C [33], and thrives within a pH range of 5 to 9 [34]. Additionally, B. halotolerans produces various beneficial compounds such as indole-related compounds, acetoin, ammonia, and indole-3-acetic acid (IAA). It also demonstrates the ability to solubilize potassium and phosphorus, as well as produce siderophores, chitinase, cellulase amylase, protease, ACC deaminase, and hydrogen cyanide [35,36]. These attributes contribute to its adaptability across various environmental conditions [31].
B. halotolerans has a circular genome of 4.15–4.2 Mb with a guanine-cytosine content of 43.81%, encoding 4,119 genes, including 30 rRNA and 85 tRNA genes [37]. Some strains exhibit genes involved in glycine/betaine uptake and bacilysin biosynthesis, critical for its saline stress tolerance and antifungal activity [29]. Advanced phylogenetic analysis using neighbor-joining trees has confirmed the close evolutionary relationships of B. halotolerans with other Bacillus species such as B. mojavensis and B. subtilis [30].
B. halotolerans survives in extreme environments, including saline and arid soils, demonstrating remarkable resilience [20]. It has been isolated from saline soil and arid regions, exemplifying the species’ capacity to endure high salinity and alkalinity [29,37]. The Qinghai–Tibet Plateau, known for its low oxygen availability, low temperatures, and high salinity, has also been identified as a habitat for B. halotolerans [38]. Strains isolated from this region exhibited not only high stress tolerance, but also biocontrol properties against plant pathogens. B. halotolerans has been isolated from different regions of the world and is involved in the biocontrol of various crops (Figure 1).

3. Biocontrol Mechanisms of B. halotolerans

3.1. Production of Antimicrobial Compounds

One of the key mechanisms behind the biocontrol effectiveness of B. halotolerans lies in its ability to produce a broad spectrum of antimicrobial compounds (AMCs) (Figure 2). These compounds, which include both ribosomally and non-ribosomally synthesized metabolites, play a crucial role in inhibiting pathogens and reducing the damage caused by plant diseases [39]. The potential of the Bacillus species, particularly those in the B. subtilis group, to dedicate a significant portion of their genome, estimated to be 4–5%, to the biosynthesis of AMCs, highlights their importance in microbial antagonism [17]. Among the AMCs produced by B. halotolerans are lipopeptides such as surfactin, fengycin, and iturin [22]. These compounds exhibit potent antimicrobial activities, effective against a range of bacteria while showing strong antifungal properties [22,40]. However, while the ability of B. halotolerans to produce diverse AMCs is well-documented, the variability in lipopeptide composition between strains raises questions about their relative efficacy. For instance, B. halotolerans strain SpS5 synthesizes surfactin and mojavensin (Table 1), which have been shown to effectively control Rhizoctonia solani, a significant plant pathogen, under both laboratory and field conditions [41]. Similarly, strain KKD1, producing surfactin and fengycin, demonstrated its antifungal potential against Fusarium graminearum [38]. Strain Cal.l.30 has been identified as a producer of several AMCs, including bacillaene, surfactin, fengycin, mojavensin, and bacillibactin, which enhance its effectiveness against Botrytis cinerea [42]. While these findings suggest strain-dependent differences in biocontrol efficacy, comparative studies assessing how variations in AMC production influence field performance remain scarce.
In addition to lipopeptides, B. halotolerans synthesizes polyketides such as bacillaene and unique bioactive compounds like azelaic acid and L-dihydroanticapsin, the precursor to the antibiotic bacilysin (Table 1). Bacilysin is an important dipeptide with potent antibacterial and antifungal activities [42]. This diverse repertoire of antimicrobial compounds highlights the broad range of AMC production in B. halotolerans strains.
The genomic basis for AMCs production in B. halotolerans underscores its biocontrol capabilities, as evidenced by multiple strains harboring biosynthetic gene clusters (BGCs) responsible for synthesizing key antimicrobial compounds. Strain QTH8, for example, harbors genes such as srfAA, srfAB, fenD, spaS, bmyB, bacA, and ituC, enabling it to combat pathogens like Fusarium pseudograminearum, the causal agent of crown rot in wheat [22]. Similarly, strain HGR5 synthesizes bacillaene, subtilosin, and bacillibactin, which showed suppressive potential against pathogens like F. graminearum, Alternaria alternata, and Phytophthora infestans [43].
Beyond plant pathogens, certain B. halotolerans strains have demonstrated antimicrobial activity against human pathogens, emphasizing their versatile bioactive potential. For example, strain B. halotolerans VT-5 produces a variety of bioactive compounds, including phenolic derivatives and diketopiperazines, which exhibit significant antimicrobial properties against Pseudomonas aeruginosa and Staphylococcus aureus [40]. A study on the strain AQ11M9, which acts as an antagonist against the human pathogen Candida auris, identified the presence of clusters for fengycin and surfactin [44].
Apart from producing diverse AMCs such as lipopeptides, polyketides, and bacteriocins, B. halotolerans also synthesizes volatile organic compounds (VOCs), which play a crucial role in its biocontrol efficacy (Figure 2). VOCs are low-molecular-weight, naturally occurring, hydrophobic substances with the ability to diffuse through the environment, enabling long-distance effects without direct contact with the target pathogens or plants [45,46]. This property makes them particularly advantageous for biofumigation, where direct application is impractical or undesirable. VOCs produced by Bacillus species have been shown to suppress the growth of plant pathogens, stimulate plant defenses, and promote plant growth [47,48].
Table 1. Review of the efficacy of B. halotolerans strains against various plant pathogens and their modes of action on different crops.
Table 1. Review of the efficacy of B. halotolerans strains against various plant pathogens and their modes of action on different crops.
CropB. halotolerans StrainsTargeted PathogensModes of ActionReferences
TomatoRFP1, RFP10, RFP57, RFP74Alternaria spp., Bipolaris spp., F. oxysporum f.sp. lycopersici, Ascochyta sp.CWDEs, VOC and antimicrobial production[49,50]
LYSX1Root-knot nematode (Meloidogyne javanica)Induced systemic resistance (ISR), nematicidal activity[51]
Gb67-VOCs (acetoin, 2,3-butanediol), enhanced root/shoot growth, reduction of salinity stress impact[32]
Cal.l.30, Cal.f.4B. cinereaVOC-mediated suppression, production of surfactin analogs[42]
WheatNYG5M. phaseolina, R. solani, P. aphanidermatum, S. sclerotiorum, A. tumefaciensVOC production (e.g., 2-methylbutanoic acid), nematicidal activity against M. javanica[52]
KKD1-Enhanced soil fertility under saline conditions, phosphate solubilization, soil pH stabilization, nutrient cycling[23]
MSR-H4-Nitrogen fixation, phosphate solubilization, and improving root-shoot K+/Na+ ratios under saline conditions[24]
JK-25Bipolaris sorokiniana, F. oxysporum, F. graminearum, Rhizoctonia zeaeSurfactin production, CWDEs; reduced antioxidant activity; siderophore [21]
QTH8F. graminearum, B. cinerea, F. pseudograminearum, S. sclerotiorum, Phytophthora nicotianae,Iturin, surfactin, fengycin; lipopeptides biosynthesis genes; growth promotion (ISR, AMCs)[22]
MaizeB7, B18, B14-Biofilm and exopolysaccharide production, increased chlorophyll under saline conditions[53]
PotatoSpS5Rhizoctonia solaniBiofilm formation, CWDEs[41]
Q2H2F. oxysporum, F. graminearum, R.solani, Stemphylium solaniSurfactin, fengycin, bacillaene, subtilosin A; VOCs; phosphate solubilization; nitrogen fixation; IAA and NH3 and biofilm[54]
F29-3R. solaniFengycin via NRPS genes; antagonistic properties; pathogen suppression in field trials[55]
SoybeanBa2-6Heterodera glycines (soybean cyst nematode)Juvenile nematode mortality, antibiosis, ISR, root colonization[56]
PeanutB28-Benzoic acid breakdown, reduce continuous cropping stress[57]
LilyLBG-1-13Botryosphaeria dothidea, B. cinerea, F. oxysporumACC deaminase activity, IAA and siderophore production, ISR and salt/drought tolerance[58]
CottonSSVP2Soil-borne nematodesACC deaminase production, mineral solubilization (P, K), and nematicidal activity[59]
Y6MSR-H4Verticillium dahliaeβ-glucanase activity; enhanced resistance in cotton in the field[60]
Date palmBFOA1–BFOA4F. oxysporum f. sp. albedinis,
F. solani, F. acuminatum,
B. cinerea, A. alternata, Phytophthora infestans, Rhizoctonia bataticola		Antagonism via AMCs (pulegone, 2-undecanone, germacrene D); salt and drought tolerance; auxin and biofilm production; nutrient solubilization, nitrogen fixation[33]
Not specifiedHGR5F. graminearum, P. infestans,
A. alternata		Fengycin, subtilosin, bacilysin; CWDEs (chitinase, cellulase, xylanase); plastic degradation[43]
Wheat, rice, maizeLDFZ001R. solaniAntifungal activity via phosphopantetheinyl transferase (SFP) and major facilitator superfamily (MFS) genes; two chitosanases; diverse biosynthetic gene clusters (NRPS, PKS).[30]
PepperMS50-18APhytophthora capsici, F. solani, R. solani, F. oxysporumAMCs and auxin production[29]
Tomato, grapes, A. thalianaHil4B. cinereaAMCs; ISR elicitors; Mojavensin cluster; secretome extracts; promotes plant growth and mitigates gray mold disease[35]
Common beanIcBac2.1R. solani, F. oxysporum,
S. sclerotiorum		Amphiphilic compounds with inhibitory activity; field efficacy against S. sclerotiorum; plant growth promotion[61]
ApplePl7B. dothideaCWDEs production, induction of plant secondary metabolite biosynthesis and plant-pathogen interaction[34]
RiceAD9-High NH3 and phosphate solubilization; salinity reduction via enzymes (SOD, CAT)[62]
StrawberriesKLBC XJ-5B. cinereaEnhancement of disease resistance compounds (phenols, flavonoids), induction of plant defense enzymes (polyphenol oxidase, phenylalanine ammonia lyase)[26]
Not specifiedDMC8R. solani, P. aphanidermatum, M. phaseolinaCWDEs (protease, chitinase), siderophores, NH3, IAA; nitrogen fixation; phosphate solubilization.[2]
VOCs have been shown to inhibit the growth of multiple fungal and bacterial plant pathogens, including Macrophomina phaseolina, R. solani, Pythium aphanidermatum, Sclerotinia sclerotiorum, Agrobacterium tumefaciens, Xanthomonas campestris, Clavibacter michiganensis, and Pseudomonas syringae [52]. Analyzing VOC profiles of B. halotolerans has revealed a range of bioactive compounds. VOCs such as 2-methylbutanoic acid and 2,3-hexanedione were identified as primary contributors to these inhibitory effects, with the latter exhibiting strong nematicidal activity against Meloidogyne javanica [52].
Beyond pathogen suppression, B. halotolerans VOCs contribute to plant growth and stress resilience. Strain Gb67 produces 3-hydroxy-2-butanone (acetoin) and 2,3-butanediol, which are associated with stress-induced defense regulation and plant growth promotion under salinity stress [32]. Additionally, strain Cal.l.30 has demonstrated VOC-mediated suppression of B. cinerea, attributed to compounds such as C13 and C15 surfactin analogs [42]. Moreover, B. halotolerans B-4359 produced VOCs that demonstrated significant efficacy against the mycelial growth of Colletotrichum acutatum [27]. The diversity and bioactivity of VOCs enable B. halotolerans to target a wide spectrum of pathogens [52]. VOCs produced by B. halotolerans not only inhibit the growth of pathogens, but also enhance plant physiological traits, such as root and shoot length, biomass, and photosynthetic ability. These effects are often attributed to the production of VOCs in conjunction with other plant growth promoting traits like ACC-deaminase activity and exopolysaccharide production [32]. The ability of B. halotolerans to produce VOCs is further exemplified in its environmental adaptability. When cultured in various growth media, its VOC profiles adapt to the conditions, producing compounds like 2-ethyl-1-hexanol and 6-methyl-2-heptanone, which demonstrate flexibility and effectiveness across diverse agricultural settings [52].

3.2. Cell Wall Degrading Enzymes

The activity of hydrolytic cell wall degrading enzymes (CWDEs) is a cornerstone of the biocontrol potential of B. halotolerans (Figure 2) [63]. These enzymes directly target and degrade the structural components of pathogen cell walls, thereby inhibiting the growth and development of harmful microorganisms [64]. The arsenal of hydrolytic CWDEs produced by B. halotolerans includes chitinases, glucanases, proteases, cellulases, lipases, and amylases, each playing a certain role in pathogen suppression [63].
Chitinases, one of the most prominent enzymes produced by B. halotolerans, are particularly effective against fungal pathogens. They hydrolyze β-(1,4)-glycosidic bonds in chitin, a critical component of fungal cell walls, producing N-acetylglucosamine and other oligosaccharides, which in return disrupt cell wall integrity [26]. The breakdown products of chitin also act as elicitors of plant defense, inducing systemic resistance against further pathogen attacks [63,65]. Glucanases, particularly β-1,3-glucanases, complement chitinase activity by degrading glucans, another key component of fungal cell walls, further weakening fungal structures and facilitating cell lysis [34].
Proteases produced by B. halotolerans target glycoproteins in pathogen membranes, while cellulases and lipases break down cellulose and lipids, respectively, attacking structural and metabolic components of pathogens [63]. The multifunctional nature of these enzymes enables B. halotolerans to combat a diverse array of plant pathogens, including fungal, bacterial, and oomycete species [26,63]. For example, the Pl7 strain of B. halotolerans with remarkable antagonistic effects against Botryosphaeria dothidea, the causal agent of apple ring rot, exhibited antifungal activity through the production of CWDEs, including protease, β-1,3-glucanase, and cellulase [34]. Another strain, KLBC XJ-5, has been reported to produce high levels of chitinase, supported by the presence of the glycoside hydrolase 18 (GH18) family chitinase genes, highlighting its ability to suppress fungal pathogens [26].
The enzymatic versatility of B. halotolerans is further demonstrated by its adaptability to environmental conditions. For example, strain DS5 produces alkaline protease (Prot DS5), which is particularly effective in high-pH environments, while strain RFP74 shows enhanced amylase production, enabling it to target starch-rich residues often associated with fungal spore development [31,50]. Lipase activity in strains like VSH 09 and RCPS2 has also been documented, providing additional biocontrol mechanisms against pathogens that rely on lipid-based cellular components [66].
Beyond pathogen suppression, the CWDEs of B. halotolerans contribute significantly to plant health and growth. Hydrolytic enzymes like cellulase and β-glucosidase enhance carbon cycling in the soil, while protease and phosphatase release nitrogen and phosphorus, enriching soil nutrient availability [65]. These dual benefits of pathogen suppression and plant growth promotion make B. halotolerans a highly versatile biocontrol agent.
Additionally, hydrolytic enzyme activity has been linked to the ability of B. halotolerans to form robust biofilms on plant roots, enhancing colonization and persistence in the rhizosphere. This property enables the sustained release of enzymes in close proximity to pathogens, maximizing their biocontrol efficacy while indirectly promoting plant growth [63].

3.3. Root Colonization and Competition for Space and Nutrients

The ability of B. halotolerans to compete with other microorganisms and efficiently colonize plant roots is fundamental to its role as a biocontrol agent (Figure 2). Root colonization ensures the bacterium’s proximity to the plant, enabling direct interactions with pathogens and promoting plant health [67]. Tian et al. emphasized the importance of efficient root colonization for beneficial rhizobacteria, allowing them to exert plant growth promoting and protective effects [68]. Additionally, Li et al. identified robust root colonization as a critical factor for the biocontrol of soil-borne pathogens such as Verticillium dahliae, a causal agent of verticillium wilt in cotton [67]. Plants actively recruit beneficial bacteria in the rhizosphere by secreting specific compounds, for example strigolactones, amino acids, and flavonoids in their exudates, which attract microbes like B. halotolerans [69,70,71].
In addition, B. halotolerans exhibited strong biofilm-forming capabilities, a trait that significantly enhances its root colonization potential [72]. Biofilms are structured communities of bacterial cells embedded in a self-produced extracellular polymeric matrix, which protects the bacteria from environmental stresses and helps in the adhesion to surfaces, including plant roots [73]. Biofilms formed by Bacillus spp. can protect plants against pathogens and improve plant resilience to abiotic stresses [72]. The biofilm production by B. halotolerans has been associated with increased tolerance to salinity, as observed in strains such as B7 and B18, which formed robust biofilms under salt stress [53].
The release of Extracellular Polymeric Substances (EPS) also plays a critical role in root colonization. EPS helps bacteria adhere to root surfaces, improves soil aggregation, and enhances the plant’s water and nutrient uptake [74]. In saline conditions, EPS can bind toxic ions like Na+, restricting their influx into plant roots and promoting water retention [75]. Additionally, B. halotolerans was reported to produce EPS with antibacterial activity against Pseudomonas aeruginosa and Serratia marcescens [76].
Competition with other microorganisms is another essential aspect of B. halotolerans’ biocontrol mechanism. By rapidly colonizing root surfaces and forming biofilms, B. halotolerans can outcompete harmful pathogens for space and nutrients [77]. Additionally, root exudates can stimulate the production of antimicrobial compounds and surfactants, further aiding in the displacement of competitors. Surfactin production has been shown to trigger biofilm formation by B. subtilis UMAF6614 and enhance the bacterium’s colonization capacity [78].

4. Plant Growth-Promoting Effect of Bacillus halotolerans in Alleviating Abiotic and Biotic Stresses

4.1. Production of Indole-3-Acetic Acid

The production of indole-3-acetic acid (IAA), a key auxin, is a central mechanism by which B. halotolerans contributes to plant growth promotion [79] (Figure 3). This phytohormone regulates a wide range of physiological processes in plants, including cell elongation, division, and differentiation, as well as root and shoot development [80]. IAA production by rhizobacteria enhances plant growth and resilience under various environmental conditions [81] (Table 2).
Several reports documented the critical role of IAA synthesis pathways in the plant-growth-promoting properties of rhizobacteria [80,82,83]. Bacillus species utilize both tryptophan-dependent and -independent pathways for IAA biosynthesis [83]. For instance, the ipdC gene, involved in the tryptophan-dependent indole-3-pyruvic acid (IPyA) pathway, played a significant role in bacterial IAA production [82]. Mutants deficient in this gene exhibited reduced colonization capabilities and a diminished ability to promote plant growth. Furthermore, modulation of IAA production under various conditions demonstrated the versatility of Bacillus strains. For example, B. velezensis strain MOST-IAA produced the highest levels of IAA when cultured under optimized conditions with specific carbon and nitrogen sources, controlled pH, and temperature, enhancing barley root growth [81].
Similarly, B. halotolerans strains isolated from challenging environments, such as saline or heavy metal-contaminated soils, exhibited robust IAA production and other plant growth-promoting traits, such as phosphate solubilization, nitrogen fixation, and ACC deaminase production, ensuring their suitability as bioinoculants in stress-prone agricultural systems [84,85]. In addition to enhancing root and shoot development, IAA-producing B. halotolerans strains improved rhizosheath formation, as seen in barley plants under drought conditions [79]. This enhanced rhizosheath formation facilitated better water and nutrient uptake, leading to improved drought tolerance [86,87]. Furthermore, multi-trait halotolerant Bacillus strains, including B. halotolerans, mitigate salinity stress by producing IAA along with other phytohormones and stress-tolerant molecules (e.g., gibberellins, cytokinins). The iPA content in wheat, a type of adenine cytokinin that improves disease resistance and sugar content, was significantly enhanced after treatment with strain KKD1. Similarly, this strain also increased the production of GA3, the most important member of the gibberellin group, which promotes stem and leaf growth [23].
Table 2. Plant-growth-promoting mechanisms of Bacillus halotolerans.
Table 2. Plant-growth-promoting mechanisms of Bacillus halotolerans.
MechanismExample StrainsImpact on PlantsReferences
IAA productionKKD1, B-4359Drought and salinity tolerance, improved nutrient uptake[23,27]
Siderophore productionJK-25, LBG-1-13, BFOA1–BFOA4Reduced chlorosis, enhanced biomass, suppression of fungal pathogens[21,33,58]
ACC Deaminase activityB5, LBG-1-13Enhanced growth under salt/drought stress, improved water holding capacity[58,88]
Nitrogen fixationMSR-H4, SSVP2, KKD1Improved soil fertility, supported growth in nutrient-deficient environments[23,24,59]
Mineral solubilizationSSVP2, AD9Enhanced nutrient uptake, stabilized soil pH[59,62]
K+/Na+ balanceMSR-H4Improved salt tolerance, reduced salinity[24]
Antioxidant enzyme inductionKLBC XJ-5Minimized cellular damage, enhanced plant resilience[26]

4.2. Siderophore Production

Siderophores, low-molecular-weight iron-chelating molecules, are critical secondary metabolites produced by a wide range of microorganisms, including B. halotolerans, to enhance plant growth under iron-limited conditions [89] (Figure 3). These compounds bind ferric iron (Fe3+) in the rhizosphere, increasing its solubility and facilitating its uptake by plants. This mechanism is particularly beneficial in iron-deficient soils, such as calcareous and alkaline environments, where the availability of ferric iron is limited [90].
The siderophores produced by B. halotolerans and related species, such as bacillibactin and catecholate-type siderophores, have been widely documented for their role in promoting plant growth and controlling pathogens. Notably, B. halotolerans JK-25 produces siderophores that inhibit the fungal pathogen Bipolaris sorokiniana and improve wheat growth under stress conditions [21]. Similarly, strain LBG-1-13 demonstrates siderophore production alongside phosphate solubilization and ACC deaminase activity, enhancing the growth of lily plants under salt and drought stress [58]. These strains not only improve iron bioavailability, but also promote the uptake of other essential nutrients by solubilizing phosphate or producing EPS contributing to sustainable agricultural practices [91]. While numerous studies have highlighted the benefits of siderophore production in agricultural applications, it is essential to critically evaluate the sustainability of these effects and their long-term impact on nutrient cycling.
In addition to nutrient facilitation, most siderophore-producing B. halotolerans strains possess antifungal properties, as seen with B. halotolerans Jk-25 against B. sorokiniana and other soil-borne pathogens, and BFOA1–BFOA4, which targets pathogens like B. cinerea and A. alternata [21,33]. Under drought and salinity conditions, siderophore production helps in mitigating stress impacts by improving root architecture, maintaining soil moisture, and enhancing micronutrient uptake [36].

4.3. ACC Deaminase Activity

The production of 1-aminocyclopropane-1-carboxylate (ACC) deaminase can lead to plant growth promotion, especially under abiotic stress conditions (Figure 3). ACC deaminase catalyzes the breakdown of ACC, the direct precursor of ethylene in plants, into α-ketobutyrate and ammonia [92]. This activity reduces ethylene levels, which are often elevated under adverse stress conditions like salinity, drought, and heavy metal, thereby alleviating the growth-inhibitory effects of ethylene [93]. By exhibiting ACC deaminase activity, B. halotolerans promotes plant growth under salt and drought stress, with notable improvements in root and shoot development in plants cultivated under these conditions [58]. An example of a strain of B. halotolerans isolated from salt-contaminated soils, expressing robust ACC deaminase activity, further confirms their potential as stress-alleviating bioinoculants [88]. The role of ACC deaminase in plant stress response is supported by its impact on physiological parameters [84]. ACC deaminase activity has been linked to increased chlorophyll content, enhanced root and shoot biomass, and improved osmotic balance under salinity stress [84,92]. In maize plants treated with B. halotolerans, stress-induced ethylene levels were reduced, leading to better water retention and improved nutrient uptake [93].

4.4. Nitrogen Fixation and Mineral Solubilization

B. halotolerans has the ability to fix atmospheric nitrogen and solubilize essential minerals, such as phosphorus, potassium, and zinc [20,23,24]. These traits enable the bacterium to enhance soil fertility and provide plants with bioavailable nutrients under both normal and stress conditions [94]. Nitrogen fixation is a crucial process that converts atmospheric nitrogen into ammonia, a form usable by plants [94,95]. Extremophilic strains of B. halotolerans have been identified as nitrogen-fixing bacteria due to the presence of the nitrogenase enzyme [20]. These strains, isolated from diverse environments, have demonstrated the ability to enhance soil nitrogen levels and contribute to plant growth even under saline and nutrient-deficient conditions [20,24].
In addition to nitrogen fixation, B. halotolerans exhibits strong mineral solubilization activities (Figure 3). The production of phosphatases by B. halotolerans converts insoluble phosphate into soluble forms like H2PO4−, enhancing its availability for plant uptake, especially under saline conditions [23,59]. Other strains, for example AD9, have been shown to solubilize phosphate even at high salt concentrations, further highlighting the salt tolerance of this bacterium [62]. Potassium and zinc solubilization are additional characteristics observed in some strains of B. halotolerans. The solubilization of potassium and zinc enhances nutrient cycling in the rhizosphere, thereby improving plant growth and health [96,97,98].
Through these mechanisms, B. halotolerans not only enhances nutrient availability, but also stabilizes soil pH, as evidenced by the strain KKD1, which maintained optimal pH levels in saline soils, creating a favorable environment for plant growth [23].

4.5. Improving K+/Na+ Balance in Plants

Maintaining an optimal K+/Na+ balance in plants is critical for mitigating salt stress and ensuring normal metabolic activities [99] (Figure 3). B. halotolerans strains have been shown to play a key role in improving ionic balance under saline conditions. For instance, plants treated with B. halotolerans demonstrated a significantly higher K+/Na+ ratio and reduced sodium accumulation in roots and shoots [100]. This improved ionic homeostasis correlates with enhanced plant growth and resilience in saline environments [24,100].

4.6. Induction of Antioxidant Enzymes

B. halotolerans is also known to elicit the production of antioxidant enzymes, which serve as the first line of defense against oxidative stress caused by abiotic and biotic stressors [101] (Figure 3). These enzymes, including superoxide dismutase (SOD), peroxidase, polyphenol oxidase, and phenylalanine ammonia lyase, have been shown to reduce the accumulation of reactive oxygen species (ROS), thereby minimizing cellular damage and enhancing plant survival under stress conditions [102]. For instance, plants treated with the strain KLBC XJ-5 of B. halotolerans exhibited significantly higher antioxidant enzyme activities, which contributed to reduced grey mold decay in postharvest strawberries and improved overall plant resilience [26].

5. Additional Applications of B. halotolerans

5.1. Nematode Management

Plant-parasitic nematodes (PPNs) are microscopic non-segmented worms that parasitize plant roots and other tissues, causing significant damage to crops worldwide. Root-knot nematodes (Meloidogyne spp.) in particular are recognized as one of the most destructive genera, responsible for severe yield losses in vegetables and cereals globally.
Species within the Bacillus genus offer promising eco-friendly solutions for nematode management. Bacillus spp. employ multiple mechanisms, including the production of VOCs, antibiotics, and enzymes, to inhibit nematode development and reproduction directly [103]. Additionally, they can enhance plant resistance to nematodes through induced systemic resistance (ISR) and biofilm formation, which acts as a physical barrier to nematode invasion [104]. B. halotolerans has shown remarkable potential as a biocontrol agent against PPNs. Recently, B. halotolerans strains demonstrated strong nematicidal activity against Meloidogyne incognita and M. javanica [51]. In the latter study, the authors found that strain LYSX1 was highly effective in inhibiting egg mass hatching and reducing juvenile nematode survival in a dose-dependent manner. Similarly, B. halotolerans strain Ba2-6 achieved 93.85% mortality of Heterodera glycines juveniles in greenhouse and field trials, highlighting its efficiency as a BCA for soybean crops [56]. In tomato, B. halotolerans not only suppressed nematode populations, but also enhanced plant growth and yield [105]. The effectiveness of B. halotolerans in nematode management is attributed to its ability to produce nematicidal compounds and induce systemic resistance in plants. These compounds disrupt nematode development, interfere with feeding site formation, and suppress reproduction [106].

5.2. Bioremediation

Heavy metals are persistent environmental pollutants due to their non-biodegradable nature and ability to accumulate in ecosystems, posing serious threats to both plant and human health [107]. They originate from both natural sources, such as soil erosion and volcanic activity, and anthropogenic sources, such as mining, fossil fuel combustion, and industrial waste [108]. Bioremediation is an eco-friendly and cost-effective approach to mitigate environmental contamination caused by toxic substances such as heavy metals, hydrocarbons, and aromatic pollutants. This process includes the ability of microorganisms to detoxify or degrade harmful contaminants through mechanisms such as biosorption, bioaccumulation, and bioprecipitation [109]
The bacillus species, known for their tolerance and ability to grow in extreme conditions, are widely studied for bioremediation. They degrade hydrocarbons, solubilize heavy metals, and restore soil fertility [109]. Strains of B. halotolerans have been identified as potent degraders of crude oil and benzoic acid, demonstrating their ability to effectively bioremediate hydrocarbon-contaminated soils [110] and mitigate the harmful effects of pollutants in soils [57].

6. Conclusions and Future Perspectives

B. halotolerans has emerged as a versatile and promising PGPR and BCA, particularly under challenging conditions such as salinity stress. Its ability to produce phytohormones, volatile organic compounds, hydrolytic enzymes, and stress regulators like ACC-deaminase and exopolysaccharides emphasize its potential in enhancing crop productivity and soil health. Additionally, members of B. halotolerans demonstrate significant applications in the bioremediation of heavy metals and other environmental pollutants, positioning it as an eco-friendly solution to mitigate soil and water contamination as well as restore ecosystem balance.
However, while numerous studies highlight its efficacy under controlled laboratory conditions, further research is needed to establish its full potential under natural and field settings. Rigorous pot and field trials are crucial to validate its biocontrol and growth-promoting efficiency across different crops and environmental conditions [32,59]. To date, only two plant biofertilizer products based on B. halotolerans strains have been identified on the market, BALANS B® by Bacillomix and PhylloZone® by EnviroKure.
Like other BCAs, the use of B. halotolerans faces challenges, including the limited expression of its full efficacy under field conditions, attributed to insufficient information on the specific modes of action of the strains employed. In addition, higher production costs remain significant drawbacks, as seen with many biopesticides. For B. halotolerans and other microbial-based products to be registered and authorized for commercial use, extensive safety studies must be conducted for regulatory risk assessments. A major challenge in this process is the effect on non-target organisms, where results are often inconsistent or difficult to interpret [111]. Additionally, the absence of standardized guidelines for assessing the unique biological properties of microbial agents further complicates the regulatory process [112]. Despite increasing demand from farmers and consumers, along with political initiatives in the EU to promote low-risk PPPs, the number of microbial-based alternatives like B. halotolerans on the European market remains limited compared to synthetic agrochemicals [113].
Future research should also focus on unraveling the molecular mechanisms underlying plant-microbe interactions, particularly in response to abiotic and biotic stressors, to enhance our understanding of their “molecular dialogue” [114]. This knowledge will pave the way for designing innovative microbial formulations and bioinoculants tailored for saline soils, bioremediation, and disease management [115,116]. The use of advanced technologies, such as next-generation sequencing (NGS), will allow researchers to uncover the complex biodegradation pathways and stress alleviation mechanisms of B. halotolerans [109]. By integrating B. halotolerans into sustainable agricultural practices, its applications as biofertilizers, biopesticides, and phytoremediators can mitigate the adverse effects of salinity, enhance crop resilience, and improve soil fertility. The continuous exploration of this bacterium holds great promise for addressing global challenges in food security and environmental sustainability.

Author Contributions

Conceptualization, P.R. and A.E.-H.; methodology, P.R.; validation, A.E.-H.; resources, R.T.V. and A.E.-H.; data curation, P.R.; writing—original draft preparation, P.R. and A.E.-H.; writing—review and editing, A.E.-H. and R.T.V.; visualization, P.R. and A.E.-H.; supervision, A.E.-H. and R.T.V.; project administration, R.T.V.; funding acquisition, R.T.V. and A.E.-H. All authors have read and agreed to the published version of the manuscript.

Funding

P.R. received a grant from the Deutscher Akademischer Austauschdienst (DAAD), grant number 57693450. The APC was funded by a 100% feature paper discount for A.E.-H.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
ACC1-aminocyclopropane-1-carboxylate
AMCsAntimicrobial Compounds
BCABiological Control Agent
BGCsBiosynthetic Gene Clusters
CATCatalase
cPPPsChemical Plant Protection Products
CWDEsCell Wall Degrading Enzymes
EPSExtracellular Polymeric Substances
FBCCFreshwater Bioresources Culture Collection
IAAIndole-3-Acetic Acid
IPMIntegrated Pest Management
ISRInduced Systemic Resistance
LBLuria-Bertani Medium
MFSMajor Facilitator Superfamily
NGSNext Generation Sequencing
NRPSNon-Ribosomal Peptide Synthetases
PALPhenylalanine Ammonia-Lyase
PGPBPlant Growth-Promoting Bacteria
PKSPolyketide Synthase
PPNsPlant-Parasitic Nematodes
POXPeroxidase
PPOPolyphenol Oxidase
ROSReactive Oxygen Species
rRNARibosomal Ribonucleic Acid
SODSuperoxide Dismutase
tRNATranfer Ribonucleic Acid
TSATryptic Soy Agar
VOCsVolatile Organic Compounds

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Figure 1. Global geographic distribution of B. halotolerans strains and their biocontrol of plant pathogens on the associated crops. (Created in Adobe Illustrator 27.6.1).
Figure 1. Global geographic distribution of B. halotolerans strains and their biocontrol of plant pathogens on the associated crops. (Created in Adobe Illustrator 27.6.1).
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Figure 2. Mechanisms of action of B. halotolerans against phytopathogens. (Created in BioRender. https://BioRender.com/ssdj7oe) (accessed on 25 January 2025).
Figure 2. Mechanisms of action of B. halotolerans against phytopathogens. (Created in BioRender. https://BioRender.com/ssdj7oe) (accessed on 25 January 2025).
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Figure 3. Actions of B. halotolerans in plant growth promotion and mitigating abiotic and biotic stresses. Key processes include the production of EPS to stabilize soil and reduce salt stress, synthesis of phytohormones like indole-3-acetic acid (IAA) to enhance root architecture, and the modulation of the K+/Na+ balance to prevent ion toxicity. Additional mechanisms, such as nitrogen fixation, phosphate solubilization, and siderophore production, improve nutrient availability and uptake, while biofilm formation aids in root colonization, protecting plants from abiotic stress and boosting growth. (Created in BioRender. https://BioRender.com/ea7j7s2) (accessed on 25 January 2025).
Figure 3. Actions of B. halotolerans in plant growth promotion and mitigating abiotic and biotic stresses. Key processes include the production of EPS to stabilize soil and reduce salt stress, synthesis of phytohormones like indole-3-acetic acid (IAA) to enhance root architecture, and the modulation of the K+/Na+ balance to prevent ion toxicity. Additional mechanisms, such as nitrogen fixation, phosphate solubilization, and siderophore production, improve nutrient availability and uptake, while biofilm formation aids in root colonization, protecting plants from abiotic stress and boosting growth. (Created in BioRender. https://BioRender.com/ea7j7s2) (accessed on 25 January 2025).
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Rafanomezantsoa, P.; El-Hasan, A.; Voegele, R.T. Potential of Bacillus halotolerans in Mitigating Biotic and Abiotic Stresses: A Comprehensive Review. Stresses 2025, 5, 24. https://doi.org/10.3390/stresses5020024

AMA Style

Rafanomezantsoa P, El-Hasan A, Voegele RT. Potential of Bacillus halotolerans in Mitigating Biotic and Abiotic Stresses: A Comprehensive Review. Stresses. 2025; 5(2):24. https://doi.org/10.3390/stresses5020024

Chicago/Turabian Style

Rafanomezantsoa, Pelias, Abbas El-Hasan, and Ralf Thomas Voegele. 2025. "Potential of Bacillus halotolerans in Mitigating Biotic and Abiotic Stresses: A Comprehensive Review" Stresses 5, no. 2: 24. https://doi.org/10.3390/stresses5020024

APA Style

Rafanomezantsoa, P., El-Hasan, A., & Voegele, R. T. (2025). Potential of Bacillus halotolerans in Mitigating Biotic and Abiotic Stresses: A Comprehensive Review. Stresses, 5(2), 24. https://doi.org/10.3390/stresses5020024

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