Introduction

In the face of mounting concerns regarding the ecological and health implications of chemical pesticides, there has been a notable shift toward exploring sustainable alternatives in agricultural and environmental research (Fan et al. 2018). The escalating interest in biocontrol agents has spurred to significant attention toward harnessing the antagonistic potential of Bacillus velezensis against a wide array of phytopathogenic fungi (Yang et al. 2020; Cheffi Azabou et al. 2020; Torres et al. 2020; Joly et al. 2021; El-Sersawy et al. 2021; Platel et al. 2021; Medhioub et al. 2022; Soliman et al. 2022). The surge in interest is underscored by the urgent need to develop eco-friendly and sustainable strategies for managing plant diseases while minimizing the use of synthetic chemicals.

Formerly known as B. amyloliquefaciens subsp. plantarum, B. velezensis is a Gram-positive, rod-shaped bacterium belonging to the B. subtilis group (Fan et al. 2018; Khan et al. 2020; Zaid et al. 2022). Widely distributed ecologically, B. velezensis has been isolated from various sources, including soil, rhizosphere, and plant surfaces (Fan et al. 2018; Khan et al. 2020). Demonstrating adaptability to diverse environmental conditions and interactions with a wide array of host plants, such as maize, soybean, tomato, and cotton (Yang et al. 2020), this bacterium holds promise for agricultural applications. In this study, we analyzed 47 meticulously selected complete genome sequences of B. velezensis sourced from the NCBI database, chosen based on stringent criteria to ensure comprehensive representation of the full genomes. Each genome corresponds to a distinct strain and its respective host, offering a detailed insight into the ecological associations of B. velezensis. To visually depict the relationship between strains and their respective plant hosts, we constructed a genome-derived phylogenetic tree using the resources provided by the Bacterial and Viral Bioinformatics Resource Center (BV-BRC) and visualized it using the Interactive Tree Of Life (ITOL) platform (https://itol.embl.de/) (Fig. 1).

Fig. 1
figure 1

Phylogenetic relationships among strains of B. velezensis and their respective hosts with Bacillus alcalophilus ATCC 27647 used as the outgroup. The analysis was conducted using 47 complete genome sequences, meticulously selected based on stringent criteria for full genome representation, sourced from the NCBI database. Each genome is linked to a unique strain and its associated host, providing a comprehensive overview of the ecological associations of B. velezensis. The phylogenetic tree was generated using the Bacterial and Viral Bioinformatics Resource Center (BV-BRC), with visualization facilitated by the Interactive Tree Of Life (ITOL) platform (https://itol.embl.de/)

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Additionally, B. velezensis has been reported to thrive in diverse environments like compost piles, water bodies, and plant residues (Torres et al. 2020), showcasing its resilience across a spectrum of ecological niches. Its frequent isolation from rhizospheric soils and association with the plant root microbiome highlight its potential as a beneficial plant growth-promoting bacterium (Rabbee et al. 2019). The diverse isolation sources and host interactions of B. velezensis underscore its ecological significance and potential as a valuable asset in agricultural and environmental settings. The strain presents a compelling solution owing to its capacity to outcompete phytopathogens for nutrients and niche space, as well as its ability to produce an array of antimicrobial compounds such as cyclic lipopeptides and polyketides, and elicit systemic resistance in host plants (Rabbee et al. 2019; Fazle Rabbee and Baek 2020). Moreover, its compatibility with integrated pest management practices and its favorable environmental profile further accentuate its role as a pivotal player in sustainable agriculture (Sawant et al. 2023; Chen et al. 2020; Dutilloy et al. 2024). The growing interest in B. velezensis as a biocontrol agent is mirrored by a growing body of research aimed at unraveling the intricate mechanisms underpinning its antagonistic interactions with phytopathogenic fungi. This study paves the way for the development of effective and environmentally sustainable biocontrol strategies in agricultural and environmental contexts. This burgeoning interest not only underscores the potential of B. velezensis as a biocontrol agent but also highlights the need to explore and leverage the ecological and agricultural benefits of microbial-based solutions in the pursuit of sustainable and resilient agroecosystems.

The objective of this review is to provide a thorough examination of B. velezensis’ capabilities to combat phytopathogenic fungi, with a specific emphasis on its molecular interactions with plants and fungi, particularly through cyclic lipopeptides. Additionally, it endeavors to scrutinize the agricultural applications of B. velezensis in promoting crop health and reducing reliance on chemical pesticides. By addressing challenges like formulation optimization and regulatory considerations, the study intends to highlight the crucial role of B. velezensis as a multifaceted ally in contemporary agricultural and industrial practices.

The taxonomic evolution of Bacillus velezensis

Bacillus velezensis was initially characterized by Ruiz-García et al. (2005) following the discovery of novel lipopeptides in a screening of environmental isolates (Ruiz-García et al. 2005). Since its identification, the taxonomic classification of B. velezensis has been a subject of considerable debate and scrutiny within the scientific community. Originally identified as a distinct species within the B. subtilis group, the taxonomic status of B. velezensis has been a matter of ongoing re-evaluation and re-classification. Due to its close resemblance to B. amyloliquefaciens, it was subsequently deemed a later heterotypic synonym of B. amyloliquefaciens by Wang et al. (2008), based on multiple analyses including DNA sequence similarities and DNA–DNA hybridization experiments (Wang et al. 2008). Through genetic analysis, the authors found that the gyrB gene sequences of B. velezensis BCRC 17467 and B. amyloliquefaciens BCRC 14193 strains formed a phylogenetic grouping, indicating their close relationship. This finding was corroborated by phenotypic analyses, which demonstrated shared morphological, physiological, chemotaxonomic, and phylogenetic characteristics between the two taxa. Consequently, B. velezensis was affiliated with B. amyloliquefaciens. However, through comparison analysis process over decades, B. amyloliquefaciens species were then clustered into two “subspecies”: B. amyloliquefaciens subsp. plantarum and B. amyloliquefaciens subsp. amyloliquefaciens (Hossain et al. 2015). Bacillus amyloliquefaciens subsp. plantarum was reported as a distinct ecotype of plant-associated B. amyloliquefaciens strains which should be considered as a later heterotypic synonym of B. velezensis (Borriss et al. 2011; Dunlap et al. 2015; Fan et al. 2017). In their study, Borriss et al. (2011) highlighted that although the strains FZB42 and DSM7 shared similar phenotypic traits, they displayed differences in DNA sequences encoding genes such as 16S rRNA, gyrase subunit A (gyrA), and histidine kinase (cheA). Later, in 2016, Dunlap and colleagues proposed that B. methylotrophicus, B. amyloliquefaciens subsp. plantarum, and B. oryzicola could be regarded as heterotypic synonyms of B. velezensis, while B. amyloliquefaciens subsp. amyloliquefaciens remained distinct. Subsequently, B. amyloliquefaciens subsp. plantarum, B. methylotrophicus, and B. oryzicola were eventually reclassified as strains of B. velezensis (Dunlap et al. 2016).

Additionally, distinctions in their enzymatic and metabolic profiles have been noted (Chun et al. 2019). Bacillus velezensis, for instance, demonstrates a broader enzymatic repertoire, including cellulases, proteases, and lipases, thereby enhancing its metabolic adaptability. This enzymatic diversity holds significant implications for various industrial application, including biofuel production, waste remediation, and food processing (Deb et al. 2013; Ngalimat et al. 2021; Alenezi et al. 2021; Diabankana et al. 2022).

Genes associated with secondary metabolite biosynthesis are more prevalent in B. velezensis, while those related to energy metabolism show enrichment in B. amyloliquefaciens (Chun et al. 2019; Ngalimat et al. 2021). Moreover, B. velezensis exhibits heightened genetic content related to the synthesis of antimicrobial compounds and genes associated with D-galacturonate and D-fructuronate metabolism in contrast to B. amyloliquefaciens and B. siamensis (Ngalimat et al. 2021). Moreover, Rückert et al. (2011) pointed out the presence of an operon involved in xylan degradation (xylA, xynP, xynB, xylR) in B. subtilis and B. velezensis FZB42, contrasting with B. amyloliquefaciens DSM7. An analysis comparing the B. amyloliquefaciens Y2 genome with other B. amyloliquefaciens genomes identified 130 genes unique to subsp. plantarum, absent in subsp. amyloliquefaciens (Rückert et al. 2011).

Therefore, the ongoing reevaluation and reclassification of B. velezensis stem from its notable genetic and phenotypic resemblance to other closely related species, particularly B. amyloliquefaciens (Dunlap et al. 2016). The delineation of B. velezensis from related species is essential for accurate species identification, ecological studies, and the development of targeted applications in agriculture and biotechnology (Adeniji et al. 2019). Nonetheless, the current classification remains a significant limiting factor for comprehensively understanding Bacillus ecology, as many strains remain misclassified in databases.

Interactions at molecular level between Bacillus velezensis, plants, and phytopathogenic fungi

At the molecular level, B. velezensis engages in complex interactions with plants, where plant immunity plays a crucial role in facilitating root or rhizosphere colonization by the bacterium. Plants release nutrient-rich root exudates, which serve as chemoattractants, creating a conducive environment for beneficial microbes to thrive (Upadhyay et al. 2022; Hao et al. 2023). The response of rhizobacteria to these exudates involves complex chemotactic mechanisms, mediated by receptors such as chemotaxis receptors and quorum sensing systems (Aroney et al. 2021). Chemotaxis receptors enable B. velezensis to detect chemical gradients in the rhizosphere, guiding its movement toward nutrients and signaling molecules released by plant roots (Feng et al. 2021).

Quorum sensing systems further facilitate communication among B. velezensis and neighboring bacterial cells, allowing for coordinated responses to changes in the host environment, which are essential for its role as a plant growth-promoting rhizobacterium (Shao et al. 2023). Two-component signal transduction systems, consisting of sensor histidine kinases and response regulators, play a crucial role in perceiving signals from plants and adjusting gene expression accordingly (Fig. 2). Upon detection of specific stimuli, sensor histidine kinases undergo autophosphorylation, initiating a cascade of intracellular signaling events that modulate gene expression.

Fig. 2
figure 2

Sequential events that take place in the rhizosphere following the application of biocontrol agent B. velezensis. The process initiates with the root colonization of B. velezensis facilitated by (i) chemotaxis, (ii) root surface attachment, and subsequent (iii) biofilm formation. Root exudates serve as signals, nutrients, and antimicrobial compounds during the colonization process. Environmental cues trigger the autophosphorylation of the histidine kinase (HK) on a histidine residue, activating a two-component signal transduction pathway. Subsequently, the phosphate group from the histidine is transferred to an aspartate residue on a response regulator (RR), leading to the phosphorylated RR acting as a transcription factor to induce the expression of genes responsive to the stimuli. These molecular reactions commonly result in the activation of a downstream MAP kinase cascade, which, in turn, stimulates the expression of transcription factors regulating genes involved in cellular responses to environmental changes. The antimicrobial compounds produced by B. velezensis exhibit antagonistic effects on pathogenic microbes within the rhizosphere (iv) while simultaneously eliciting plant growth promotion and enhancing defense responses in plants (v)

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In the context of tripartite interactions, fungal hyphae release compounds that elicit chemotactic responses from rhizobacteria, contributing to the establishment of an underground “fungal highway” around plant roots. These interactions underscore the complexity of molecular communications between B. velezensis, plants, and phytopathogenic fungi, highlighting the importance of understanding these mechanisms for agricultural and biotechnological applications. After B. velezensis establishes interaction with the plant, the plant’s pattern-recognition receptors (PRRs) identify specific molecules known as microbe-associated molecular patterns (MAMPs) produced by the rhizobacteria (Boller and Felix 2009). This recognition initiates a cascade of biochemical and genetic responses in the plant, triggering the activation of defense pathways and ultimately limiting pathogen proliferation (Fan et al. 2018; Rabbee et al. 2019; Akintayo et al. 2023).

Bacillus velezensis strains have been shown to regulate pathogen proliferation by balancing plant hormone levels, as demonstrated by B. velezensis FZB42. The colonization of plant roots by this strain prevents the entry of foliar pathogens such as Nicotiana benthamiana through stomata by activating the abscisic acid (ABA) and salicylic acid (SA)-regulated pathways, which induce stomatal closure post-pathogen infection (Wu et al. 2018). By modulating plant hormones, beneficial strains can improve plant growth, particularly by stimulating auxin, cytokinin, or gibberellin production while inhibiting ethylene production through 1-aminocyclopropane-1-carboxylate deaminase (ACC deaminase) activity (Santner et al. 2009). For instance, B. velezensis BACO3 was found to increase radish root and leaf weights, likely due to its production of indole-3-acetic acid and ammonia, as well as its ACC deaminase activity (Meng et al. 2016). Another example is B. velezensis FZB42, which has been demonstrated to produce IAA (Idris et al. 2007). Moreover, in the interactions between B. velezensis, plants, and phytopathogenic fungi, a multifaceted communication network exists at the molecular level. This communication involves the secretion of cyclic lipopeptides (CLiPs) by B. velezensis, serving as signaling molecules that can trigger plant defenses, acting as antagonists against phytopathogens, and modulating various biological processes (Lam et al. 2021; Anckaert et al. 2021; Platel et al. 2022).

Bacillus velezensis bioactive metabolites: unveiling the role of polyketides and cyclic lipopeptides

Bacillus velezensis is known for its capacity to produce a diverse array of bioactive metabolites, with approximately 5–8% of its genome dedicated to synthesizing antimicrobial compounds such as volatile organic compounds (VOCs), bacteriocins, hydrolase enzymes, polyketides (PKs), and cyclic lipopeptides (CLiPs) (Chen et al. 2007; Ongena and Jacques 2008; Chun et al. 2019; Anckaert et al. 2021). Several studies have already highlighted the vital role of the VOCs in both stimulating plant growth and exerting anti-pathogenic effects. For instance, B. velezensis G341 could inhibit the mycelial growth of various phytopathogenic fungi by producing dimethyl sulfoxide, 1-butanol, and acetoin, while B. velezensis BAC03 enhances the growth of several crops through the production of acetoin and 2,3-butanediol (Lim et al. 2017; Meng et al. 2016).

Bacillus velezensis exerts its plant protection effect through the production of polyketides (pKs) and cyclic lipopeptides (CLiPs). These CLiPs are amphiphilic molecules featuring a hydrophilic peptide part and a lipophilic lipid part, which contribute to their antifungal properties. Both PKs and CLiPs share the common characteristic of not being produced by ribosomes but assembled by enzymatic complexes known as polyketide synthases (PKS) and nonribosomal peptide synthetases (NRPSs), respectively.

NRPSs are megaenzymes organized into modules composed of adenylation (A), thiolation (T), and condensation (C) domains, with each module responsible for recognizing, activating, and connecting specific amino acid to produce the final peptide (Gao et al. 2018; Challis and Naismith 2004; Weber and Marahiel 2001). These basic domains can be extended by substrate-modifying domains, including domains for substrate epimerization, β hydroxylation, N methylation, and heterocyclic ring formation. Finally, the last module includes the thioesterase (Te) domain responsible for removing the fully assembled peptide from the T domain in the ultimate module (Challis and Naismith 2004). In some circumstances, the Te domain can participate in an intramolecular reaction that results in the formation of a cyclic or partially cyclic peptide.

Compared to polypeptides produced by ribosomal peptide biosynthesis, the primary structure of NRPs is mainly partially or totally cyclic, and the biodiversity of monomers is not limited to the 20 proteogenic amino acids residues. These monomers can include modified versions such as 2-aminoisobutyric acid, hydroxyphenylglycine, and 2,3-dihydroxybenzoic acid (Caboche et al. 2010).

Polyketide biosynthesis, on the other hand, requires at least four domains that can be organized into modules like to those in NRPSs. These domains include acyltransferase (AT), ketosynthase (KS), and thioesterase (Te), with additional domains such as ketoreductase (KR), dehydratase (DH), and enol reductase (ER) modifying the structure (Hertweck 2009; Esmaeel et al. 2016). Bacillus species are also capable of producing NRPS/PKS products synthesized via hybrid gene clusters containing gene encoding both NRPSs and PKs module-containing proteins, like locillomycin and bacillaene metabolites.

Among PKs, bacillaene, difficidin, and macrolactin are the main types with antibacterial properties, effective against various rice pathogens such as Xanthomonas oryzae pv. oryzae and X. oryzae pv. Oryzicola (Anckaert et al. 2021; Rabbee et al. 2019). The production of macrolactin can inhibit cell division and downregulating the transcription of chvB and chvE in Agrobacterium tumefaciens C58 (Chen et al. 2021). Additionally, other studies have also shown that bacillaene exhibits antibiotic properties and regulates biofilm formation, thereby enhancing the bacterium’s defense mechanisms (Li et al. 2021; Erega et al. 2021) (Table 1).

Table 1 Polyketides produced by B. velezensis, formula, structures, molecular masses, and activities
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The three main cyclic-lipopeptides characterized in B. velezensis are the families of iturin, fengycin, and surfactin. Notable members within the iturin family include bacillomycin, iturin, and mycosubtilin. Iturins disturb the cytoplasmic membrane, resulting in the leakage of K + ions and other cellular constituents, ultimately leading to cell death (Park et al. 2022). Fengycin compounds, on the other hand, demonstrate efficacy against filamentous fungi by interacting with sterols and phospholipids present in the fungal membrane. Deleu et al. (2005) proposed two mechanisms of action for fengycin, depending on its concentration: at low concentration, fengycin aggregates to form pores, leading to permeability changes in the membrane, while at high concentration, it acts as a detergent, solubilizing the membrane (Deleu et al. 2005). Regarding surfactin, although it may not independently exhibit a potent antifungal impact, it demonstrates synergistic action with the iturin and fengycin families, amplifying the suppression of fungal growth (Mejri et al. 2018) (Table 2).

Table 2 Cyclic lipopeptides produced by B. velezensis, formula, structures, molecular masses, and activities
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Lipopeptides are not only powerful antifungal compounds through direct action on the pathogen membrane but are also effective in stimulating induced systemic resistance (ISR) in plants. The complete mechanism of interaction between lipopeptides and the plant cells remains unclear; however, some studies have demonstrated that the recognition is not protein receptor dependent but rather involves a process based on the interaction and penetration of lipopeptides into the lipid bilayer fraction of plant membranes (Crouzet et al. 2020). Consequently, numerous strains of B. velezensis can promote plant defense reaction by stimulating the expression of plant defense genes. For instance, B. velezensis strain BE2 was able to reduce the incidence of Zymoseptoria tritici on wheat and Pyrenophora teres on barley when applied at root level (Dutilloy et al. 2024). Application of the strain BE2 before the infection at the leaf level induced an upregulation of several genes implicated in plant protection. Using ULPC-MS analyses, the authors detected the production of seven metabolite families, including the three CLiPs (Dutilloy et al. 2024). Other studies have established the role of CLiPs in inducing ISR in plant. The mutant AK3, which produces only surfactin, induced systemic resistance in ryegrass, enhancing hydrogen peroxide (H2O2) development, elevating cell wall/apoplastic peroxidase activity, and promoting the deposition of callose and phenolic/polyphenolic compounds (Fan et al. 2018). Additionally, fengycin and iturin produced by B. velezensis were found to be necessary for inducing ISR against rice blast in potting soil and acid sulfate soil conditions (Lam et al. 2021). During this study, it was noted that plants react differently to lipopeptides, likely due to differences in cell membrane composition. Peptide composition also plays a key role in biological activity. For example, lichenysin exhibits higher surfactant power than surfactin, despite the main structural difference being the presence of a glutaminyl residue in position 1 of the peptide sequence in place of glutamic acid in surfactin (Grangemard et al. 2001).

Therefore, B. velezensis strains play a pivotal role within the Bacillus species. Their multifaceted mechanisms for combating the most deleterious pathogens for crops have rendered them a very promising alternative to pesticides for the foreseeable future. Among these mechanisms, the use of cyclic lipopeptides has become a key area of research, with numerous studies focused on optimizing their application in agricultural settings.

Agricultural applications of B. velezensis

As previously discussed, extensive research supports the use of B. velezensis in the agricultural sector as a sustainable alternative to synthetic fertilizers and chemical pesticides. This beneficial bacterium is employed for its plant growth-promoting properties, including the production of antimicrobial compounds, biocontrol of plant pathogens, and enhancement of nutrient uptake, and stress tolerance in diverse crops. Its versatility and effectiveness make it as a promising candidate for sustainable agricultural practices (Table 3).

Table 3 Case studies highlighting the successful application of B. velezensis in controlling specific phytopathogenic fungi in different agricultural settings
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Bacillus velezensis strains exhibit remarkable antifungal capacity against a wide range of pathogens affecting various plant hosts. As indicated in Fig. 1, which reflects only a subset of characterized strains compared to those registered in the NCBI, B. velezensis interacts with cereals, vegetables, grapevines, and trees, effectively reducing the impact and incidence of necrotrophic (Sawant et al. 2023), biotrophic (Chen et al. 2020), or hemibiotrophic (Dutilloy et al. 2024) pathogens. These strains are particularly studied for their application in farming, as they show efficacy against major pathogens such as Fusarium graminearum, Botrytis cinerea, Plasmodiophora brassicae, or Z. tritici (Zhu et al. 2020; Asaturova et al. 2022; Li et al. 2023).

For instance, B. velezensis strain FZB42 has been shown to produce a range of secondary metabolites, such as cyclic lipopeptides previously described, which exhibit strong antifungal and antibacterial activities (Chowdhury et al. 2015). These antimicrobial compounds not only directly suppress the growth of pathogens but also induce systemic resistance in plants, enhancing their defense mechanisms against diseases (Ongena and Jacques 2008). The underlying mechanism for the inhibition was then investigated where it was shown that bacilysin played a pivotal role in inhibiting the pathogen by damaging its hyphal structures and suppressing relevant gene expression. In addition, the strain FZB42 significantly inhibited the expression of Phytophthora sojae genes related to growth, macromolecule biosynthesis, pathogenicity, and ribosomes. Among them, the genes for pectate lyase were the most significantly downregulated (Han et al. 2021). Moreover, B. velezensis FZB42 significantly inhibited Fusarium graminearum growth by producing bacillomycin D, causing structural damage to fungal hyphae and conidia (Gu et al. 2017). In this context, B. velezensis 83 synthesizes bacillomycin D in vitro, resulting in detrimental effects on the cell membranes of Colletotrichum gloeosporioides, consequently impacting its survivability (Luna-Bulbarela et al., 2018). Originally isolated from the phyllosphere of mango trees in Mexico, this particular strain exhibits efficacy similar to that of chemical treatments such as Captan 50 PH™ or Cupravit hidro™ in the efficient control of anthracnose in Kent mangoes (Balderas-Ruíz et al. 2020). Furthermore, a study highlighted that CLiPs produced by the KB21 strain serve as competent biocontrol agents against plant fungal pathogens, especially pepper anthracnose, due to the production of iturin (Park et al. 2022). Additionally, fluorescent-labeled endophytic B. velezensis CC09 demonstrated disease control efficacy of 66.67% and 21.68% against take-all disease caused by Gaeumannomyces graminis var. tritici and spot blotches of wheat leaves caused by Bipolaris sorokiniana, respectively (Kang et al. 2018). This study suggested that the antifungal activity of iturin A may result from the indirect effect of systemic resistance generated by B. velezensis CC09 in wheat plants (Kang et al. 2018). To reduce the incidence of wheat powdery mildew, Cai et al. (2017) conducted a field trial investigating the efficacy of a bioactive metabolite extract derived from B. velezensis CC09. The application of these metabolites resulted in a substantial 86.12% reduction in the severity of the mildew disease, surpassing the performance of the commercial fungicide triazolone, which achieved a 50.39% reduction when utilized as pretreatment samples (Cai et al. 2017).

Moreover, B. velezensis B5 has demonstrated significant efficacy in inhibiting cabbage fusarium wilt (CFW) caused by Fusarium oxysporum f. sp. conglutinans (Li et al. 2022). Additionally, strain YB-130, through the production of fungal cell wall degrading enzymes, markedly inhibited the growth and hyphal development of Fusarium graminearum PH-1, the causative agent of wheat scab. Furthermore, strain YB-130 exhibited a reduction in deoxynivalenol production by Fusarium graminearum PH-1 through the suppression of key genes such as tri5, tri3, and tri8, essential for deoxynivalenol production (Xu et al. 2020). Likewise, Bacillus sp. MEP2 18, a soil bacterium known for its rich reservoir of bioactive molecules, predominantly synthesizes C16–C17 fengycin and other CLiPs when cultivated under optimized conditions (Medeot et al. 2023).

Previous studies have reported that the inoculation of MEP2 18 strain significantly increased the growth of maize seedlings under normal and saline conditions. Moreover, the cell-free supernatant of MEP218 exhibits potent antifungal properties, effectively suppressing the growth of Fusarium spp. and Sclerotinia spp. This antifungal activity was attributed to the production of the iturin A C15 (Medeot et al. 2017). As for HN_Q_8 strain, it exhibits considerable potential in controlling potato common scab caused by Streptomyces scabies through the production of bacteriocin (Zhao et al. 2022). Another study highlighted its antagonistic effect on Alternaria solani, the causal agent of potato early blight, achieved through the modulation of defensive enzyme activities and the induction of the JA/ET pathway. Additionally, it promotes plant growth by regulating the contents of IAA, GA3, and ABA, enhancing the chlorophyll content, and stimulating root activity (Bai et al. 2023). Husna et al. (2023) reported the strain’s biocontrol efficacy against pathogenic contamination in lettuce hydroponics through surfactin production. Moreover, some studies have shown that endophytes can enhance host resistance to diseases. Hamaoka et al. (2021) found that the endophyte B. velezensis KOF112 induced grapevine defense responses through both salicylic acid- and jasmonic acid-dependent defense pathways. This strain had antagonistic activities against gray mold caused by Botrytis cinerea, anthracnose caused by Colletotrichum gloeosporioides, and downy mildew caused by Plasmopara viticola. Similarly, B. velezensis S3-1, isolated from the rhizosphere soil of cucumber, demonstrated inhibition of plant pathogens, promotion of plant growth, and efficient colonization of rhizosphere soils. The strain produced 13 kinds of CLiPs, including surfactin, iturin, and fengycin families (Jin et al. 2017). A recent study revealed its biocontrol potential against pepper wilt caused by Fusarium sp. F1T, achieved by inhibiting spore germination and colony growth of pathogenic fungus, enhancing the expression levels of defense enzymes genes in pepper, thereby enhancing its disease resistance (Fan et al. 2023). Furthermore, B. velezensis YYC significantly reduced the incidence of bacterial wilt in tomato plants caused by Pseudomonas solanacearum by enhancing plant basal immunity through the increased activity of defense-related genes such as PAL, POD, and SOD (Yan et al. 2022). Regarding verticillium wilt of cotton, B. velezensis AL7 efficiently inhibited the growth of Verticillium dahliae Kleb through fengycin production (Liu et al. 2021). In addition, B. velezensis GUMT319 exhibited a significant effect on grape yields (Chen et al. 2022) and remarkable biocontrol activity against tobacco black shank disease caused by Phytophthora nicotianae (Ding and Mo 2021). The strain ZY1, isolated from pepper leaves, recently demonstrated strong biocontrol efficacy against bacterial fruit blotch (BFB) of Cucurbitaceae (Ji et al. 2023). Lim et al. (2017) reported that B. velezensis strain G341, isolated from Korean ginseng roots, produces diffusible and volatile antifungal compounds effective against various phytopathogenic fungi, including those responsible for rice sheath blight, tomato gray mold, tomato late blight, wheat leaf rust, barley powdery mildew, and red pepper anthracnose (Lim et al. 2017). Additionally, Liang et al. (2021) highlighted the antimicrobial activities of B. velezensis ATR2 strain against ginger rhizome rot disease caused by Bacillus pumilus GR8. Genome analysis revealed that B. velezensis ATR2 harbors a series of genes closely related to promoting plant growth and triggering plant immunity (Liang et al. 2021).

Overall, B. velezensis offers a myriad of agricultural benefits, serving as a biocontrol agent against plant pathogens, enhancing nutrient uptake, promoting plant growth, and improving plant stress tolerance. Its effectiveness and versatility position make it as a promising candidate for sustainable agriculture practices aimed at reducing reliance on chemical inputs and enhancing crop productivity. However, further research and field trials are necessary to fully explore and harness the potential of this bacterium in agricultural systems.

Industrial and environmental applications of B. velezensis

Different strains of B. velezensis have demonstrated potential applications in the degradation of diverse toxic and hazardous industrial byproducts. One of the notable industrial applications of B. velezensis is its ability to produce enzymes of industrial interest. For instance, B. velezensis strain QST713 has been found to produce a range of enzymes, including amylases, proteases, cellulases, and lipases, which have been utilized in various industrial processes (Ngalimat et al. 2021). These enzymes have applications in the food industry for improving the processing of starch, proteins, and lipids, as well as in the production of biofuels, detergents, and other biotechnological products.

Furthermore, B. velezensis has shown promise in the field of bioremediation. This bacterium has the ability to degrade a wide range of organic pollutants, including hydrocarbons, pesticides, and aromatic compounds. For example, B. velezensis has been reported to effectively degrade polycyclic aromatic hydrocarbons (PAHs) and promote the remediation of PAH-contaminated soil (Safitri et al. 2019; Lu et al. 2020; Sultana et al. 2021). Similarly, B. velezensis strain MHNK1 has demonstrated the capability to degrade the herbicide atrazine and has potential applications in the cleanup of atrazine-contaminated environments (Jakinala et al. 2019).

Overall, the industrial and environmental applications of B. velezensis encompass enzyme production, bioremediation, production of bioactive compounds, and promotion of plant growth and soil health. The versatility and beneficial characteristics of B. velezensis make it a promising candidate for various industrial sectors, including biotechnology, environmental remediation, and agriculture. Further research and development are essential to fully exploit the potential of this bacterium and translate it into practical applications that contribute to sustainable industrial processes and environmental management.

Challenges and future perspectives

The widespread adoption of B. velezensis as a biocontrol agent faces several challenges and limitations that must be addressed for successful implementation. One key challenge lies in formulating B. velezensis-based products, similar to most bacterial-based formulations. Although several biocontrol products based on Bacillus strains, including B. velezensis, are already available on the market, ensuring the stability and viability of these products during storage and application is crucial for their effectiveness. Additionally, their efficacy can be negatively impacted by inconsistent environmental conditions such as humidity and temperature, as well as competition with native soil and plant microbiomes, leading to variable performance. Hence, developing efficient and cost-effective formulations that ensure high survival rates and prolonged shelf life remains a significant challenge (Alenezi et al. 2021; Diabankana et al. 2022).

Moreover, regulatory considerations pose hurdles to the widespread adoption. The registration and approval processes for biocontrol agents involve rigorous testing, safety assessments, and compliance with regulatory standards, which can be time-consuming and costly, impeding commercialization and accessibility (Baker et al. 2020; Sundh and Eilenberg 2021; Stenberg et al. 2021; Lahlali et al. 2022; Maral-Gül and Eltem 2024).

To overcome these challenges, future research directions and technological advancements can focus on several aspects. Firstly, optimizing the formulation of B. velezensis-based products to improve shelf life, stability, and delivery methods is imperative. Exploring encapsulation techniques, protective additives, and innovative delivery systems can enhance the survival and efficacy during application. Additionally, further studies are needed to understand the mechanisms underlying the interactions between B. velezensis, target pathogens, and host plants.

Another limitation lies in the efficacy of B. velezensis as a biocontrol agent (Thanh Tam et al. 2023). Although B. velezensis strains produce a diverse array of bioactive metabolites with significant agricultural and biotechnological applications, their production in very small quantities limits their scalability and commercial viability. Addressing this challenge requires innovative approaches such as heterologous expression and other genetic strategies. Introducing biosynthetic gene clusters responsible for metabolite production from B. velezensis into genetically tractable host can overcome limitations in native production. Notably, B. velezensis strain FZB42 has found industrial application as a biocontrol agent in various pesticides (Fan et al. 2018; Put et al. 2024).

Effective collaboration among researchers, industry stakeholders, and regulatory agencies is crucial to streamline regulatory processes. Establishing clear guidelines and standardized protocols for registration and approval of B. velezensis-based products can facilitate their commercialization and market acceptance. Overall, addressing these challenges comprehensively will enhance the biocontrol efficacy of B. velezensis and enable tailored approaches for different agricultural systems and target pathogens.

In conclusion, B. velezensis emerges as a promising candidate for sustainable agricultural practices and biotechnological applications. Its multifaceted interactions with plants and phytopathogenic fungi, coupled with its biocontrol mechanisms mediated by cyclic lipopeptides, highlight its potential as a biocontrol agent and plant growth promoter. The agricultural benefits of using B. velezensis in enhancing crop health and yield, combined with its industrial and environmental applications, highlight its versatility and economic potential. Despite a broad issue existing challenges in deployment, such as formulation complexities and regulatory hurdles, the future outlook for B. velezensis remains promising. Continued research and innovation in harnessing the full potential of this bacterium are crucial for maximizing its impact in sustainable agriculture and environmental management. Bacillus velezensis stands ready to play a pivotal role in shaping the future of agriculture and biotechnology, offering sustainable solutions to complex challenges in modern farming practices.