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Review

A Review on the Biotechnological Applications of the Operational Group Bacillus amyloliquefaciens

by
Mohamad Syazwan Ngalimat
1,
Radin Shafierul Radin Yahaya
1,
Mohamad Malik Al-adil Baharudin
1,
Syafiqah Mohd. Yaminudin
2,
Murni Karim
2,3,
Siti Aqlima Ahmad
4 and
Suriana Sabri
1,5,*
1
Enzyme and Microbial Technology Research Center, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia, Serdang 43400, Selangor, Malaysia
2
Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia, Serdang 43400, Selangor, Malaysia
3
Laboratory of Sustainable Aquaculture, International Institute of Aquaculture and Aquatic Sciences, Universiti Putra Malaysia, Port Dickson 71050, Negeri Sembilan, Malaysia
4
Department of Biochemistry, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia, Serdang 43400, Selangor, Malaysia
5
Department of Microbiology, Faculty of Biotechnology and Biomolecular Sciences, Universiti Putra Malaysia, Serdang 43400, Selangor, Malaysia
*
Author to whom correspondence should be addressed.
Microorganisms 2021, 9(3), 614; https://doi.org/10.3390/microorganisms9030614
Submission received: 22 January 2021 / Revised: 24 February 2021 / Accepted: 26 February 2021 / Published: 17 March 2021
(This article belongs to the Section Microbial Biotechnology)
Browse Figures
Versions Notes

Abstract

:
Bacteria under the operational group Bacillus amyloliquefaciens (OGBa) are all Gram-positive, endospore-forming, and rod-shaped. Taxonomically, the OGBa belongs to the Bacillus subtilis species complex, family Bacillaceae, class Bacilli, and phylum Firmicutes. To date, the OGBa comprises four bacterial species: Bacillus amyloliquefaciens, Bacillus siamensis, Bacillus velezensis and Bacillus nakamurai. They are widely distributed in various niches including soil, plants, food, and water. A resurgence in genome mining has caused an increased focus on the biotechnological applications of bacterial species belonging to the OGBa. The members of OGBa are known as plant growth-promoting bacteria (PGPB) due to their abilities to fix nitrogen, solubilize phosphate, and produce siderophore and phytohormones, as well as antimicrobial compounds. Moreover, they are also reported to produce various enzymes including α-amylase, protease, lipase, cellulase, xylanase, pectinase, aminotransferase, barnase, peroxidase, and laccase. Antimicrobial compounds that able to inhibit the growth of pathogens including non-ribosomal peptides and polyketides are also produced by these bacteria. Within the OGBa, various B. velezensis strains are promising for use as probiotics for animals and fishes. Genome mining has revealed the potential applications of members of OGBa for removing organophosphorus (OPs) pesticides. Thus, this review focused on the applicability of members of OGBa as plant growth promoters, biocontrol agents, probiotics, bioremediation agents, as well as producers of commercial enzymes and antibiotics. Here, the bioformulations and commercial products available based on these bacteria are also highlighted. This review will better facilitate understandings of members of OGBa and their biotechnological applications.

1. Introduction

In 1943, a Japanese scientist, Juichiro Fukumoto, first isolated Bacillus amyloliquefaciens from the soil. The species is named after its unique character because it produced (faciens) a liquefying (lique) α-amylase (amylo) [1,2]. Later, B. amyloliquefaciens was combined with the closely related Bacillus subtilis and Bacillus licheniformis into the B. subtilis species complex, based on phylogenetic and phenetic evidence [3]. From the B. subtilis species complex, it can be further sub-grouped into the operational group B. amyloliquefaciens (OGBa) that comprises four bacterial species; the soil-borne B. amyloliquefaciens, the plant-associated Bacillus siamensis and Bacillus velezensis, and a black-pigment-producing strain Bacillus nakamurai [4].
Previously, several bacterial species of the OGBa, namely B. amyloliquefaciens subsp. plantarum, Bacillus methylotrophicus and Bacillus oryzicola, were reclassified as strains of B. velezensis [5]. Genome-based and gene-derived phylogenetic analyses revealed that B. velezensis belongs to a conspecific group consisting of B. velezensis, B. amyloliquefaciens subsp. plantarum FZB42 (reclassified as B. velezensis FZB42) and B. methylotrophicus. However, B. velezensis is distinct from the closely related species of B. amyloliquefaciens and B. siamensis [4]. To date, a plethora of bacterial whole-genome sequences (WGS) from members of OGBa have been deposited into the National Center Biological Information (NCBI) database (Table S1). As confirmed taxonomically in 2019, 223 genomes belonged to B. velezensis, 19 belonged to B. amyloliquefaciens, 10 belonged to B. siamensis and 2 belonged to B. nakamurai [6].
The members of OGBa are found in various niches including soil, plants, food, animal faeces and aquatic environments [4]. Currently, genome mining has revealed their applicability as plant growth-promoters, biocontrol agents, probiotics, bioremediation agents as well as producers of commercial enzymes and antibiotics [7,8]. Therefore, knowledge of the biology of the OGBa is imperative to understanding the special qualities of the group. This review focused on the biotechnological applications of the bacterial strains belonging to the OGBa.

2. An Overview of the OGBa

2.1. Identification and Characterization

Bacterial species from the OGBa are all Gram-positive bacteria and motile by peritrichous flagella. They are endospore-forming bacteria from the B. subtilis species complex. For many years, the speciation of OGBa within the B. subtilis species complex has been uncertain, often leading to erroneous and variable results. They are difficult to distinguish using classical taxonomy parameters: morphological and physiological characteristics, cell wall compositions, 16S ribosomal RNA sequence, guanine–cytosine (G+C) content, fatty acid methyl esters (FAME) and DNA–DNA hybridization (DDH) [9]. Therefore, the taxonomic status of the bacterial species belonging to the OGBa is constantly causing confusion to researchers, especially for non-professional taxonomy researchers.
It is worth mentioning that some studies have used protein-coding genes in order to further ascertain the degree of relatedness of the OGBa within the B. subtilis species complex [10,11]. The highly conserved DNA gyrase subunit B (gyrB), signal transduction histidine kinase CheA (cheA) and RNA polymerase β-subunit (rpoB) were used for the study of speciation within the B. subtilis species complex before the advent of multilocus sequence analysis (MLSA) [11,12,13]. The taxonomical status of the members of OGBa has been solved by genome-based [4] and gene-derived [14] phylogeny analyses. The OGBa comprised four species: (i) B. amyloliquefaciens; (ii) B. siamensis; (iii) B. velenzensis; and (iv) B. nakamurai, as confirmed by cladistic analysis (Figure 1; Table 1).

2.2. Ecology, Isolation and Cultivation

The ability to produce endospores when facing harsh conditions allowed the members of the operational group to survive in various niches including soil, animal faeces, plants, food, bee products, drugs, air, and the aquatic environments (Table S1). Evidently, the members of OGBa had been directly isolated from rare dormant volcanic soils [19], mango orchards [20] and animal faeces [21,22]. They had also been isolated from plant parts including fruits (such as lemons [23] and apples [24]), roots (such as Peruvian ground cherry [25] and peanut roots [26]) and leaves (such as lucerne [27] and camphor leaves [28]).
Moreover, traditional fermented foods including bibimbap [29], douchi [30], and doenjang [31] were reported as the sources of isolation of bacteria from this operational group. They also were isolated from bee products [32,33,34], heroin [35], and air [36]. In other related studies, bacteria of this operational group have been isolated from water [37], seawater [38] and sea sediment [39]. Chicken [40] and fish intestines [41] were also reported as the sources of origin for members of this operational group.
Generally, the members of OGBa are cultivated routinely in Luria–Bertani (LB) medium at 30–37 °C aerobically [11,16,17]. Some members of OGBa such as B. nakamurai grew well on nutrient agar (NA), trypticase soy agar (TSA), Reasoner’s 2A agar (R2A) and tryptone glucose yeast extract agar (TGY) at 30 °C for two days [18]. Moreover, B. velezensis and B. siamensis were also reported to grow well on TSA at 37 °C and 32 °C, respectively [16,17].

2.3. Genome and Its Arrangement

In 2019, 254 bacterial strain genomes which had been deposited in the NCBI database were reported as belonging to the OGBa [6]. Some of the examined strains were found to contain plasmids (Table S1). Most of the reported strains had only one plasmid, except for B. velezensis 157, B. velezensis DKU_NT_04, and B. velezensis NJAU-Z9 (all contained two plasmids), and B. velezensis LB002 (which contained three plasmids). Interestingly, some studies have focused on the functionality of the genes carried by the plasmid. For instance, the B. velezensis S499 plasmid, pS499, was reported as containing a rap-phr cassette. This cassette encoded for the regulator aspartate phosphatase (rap) and the Rap regulatory peptide (phr) with a role in governing protease secretion, growth and motility, biofilm formation and production of surfactin [42]. Meanwhile, B. amyloliquefaciens LL3 plasmid, pMC1, has a 6.8 kbp plasmid that includes a rap which is not homologous to the pS499 [42]. The hypothetical rap and the origin of replication of the pMC1 plasmid were cloned into the pKSV7, vector which brought about the production of plasmid-cured strains. The plasmid-cured strains have increases in glutamate-independent poly-γ-glutamic acid production by 6% as compared to the B. amyloliquefaciens LL3 [43].
Genome analysis allowed for further biological studies on the members of OGBa. The genomic and metabolic features of the members of the group were similar; however, species-specific features including secondary metabolite biosynthesis-related and energy metabolism-related genes were also identified [4,44]. Secondary metabolite biosynthesis-related genes are enriched in B. velezensis, whereas energy metabolism-related genes are enriched in B. amyloliquefaciens. In the core-genome, B. velezensis harbors more genes involved in the biosynthesis of antimicrobial compounds as well as genes involved in D-galacturonate and D-fructuronate metabolisms compared to B. amyloliquefaciens and B. siamensis. Moreover, a xanthine oxidase gene cluster that is involved in metabolizing xanthine and uric acid to glycine and oxalureate was found in the core-genome of all the members of the group. Pan-genome analysis revealed the abilities of members of OGBa to metabolize diverse carbon sources aerobically or anaerobically. Their abilities to produce various metabolites such as lactate, ethanol, xylitol, diacetyl, acetoin, and 2,3-butanediol were also identified [44]. In addition, genome analysis suggested that the regions of genomic plasticity controlled the function and structure of the genome and governed the adaptations to different niches [45]. Genome analysis also enabled the prediction of uncharacterized gene clusters and assessed the capabilities of members of OGBa to produce antimicrobial compounds [6].

3. The Importance and Applications of the OGBa

3.1. Plant Growth Promoters and Biocontrol Agents in Agriculture

In the agricultural sector, the biocontrol strategy has received great attention because it provides safe, environmentally friendly, long-lasting, and inexpensive alternatives [46]. The characterizations of the bacterial strains from the OGBa as biocontrol agents were determined based on their abilities to improve plant growth and health [47]. These abilities involve multiple mechanisms including direct (improve plant growth) and indirect (improve plant health) mechanisms (Figure 2). Direct mechanisms involve nitrogen fixation, phosphate solubilization, siderophore production and phytohormone production (e.g., indole-3-acetic acid (IAA) and enzymes such as 1-amyclocyclopropane-1-carboxylate (ACC) deaminase). It has been reported that the co-inoculation of B. velezensis S141 with Bradyrhizobium diazoefficiens USDA110 into soybean resulted in enhanced nodulation and nitrogen fixation efficiency by producing larger nodules [48]. In another related study, the members of OGBa were able to solubilize phosphate, and produce IAA, ACC deaminase and siderophores [49,50,51].
Meanwhile, the indirect mechanism is mainly due to their biocontrol activities attributed to the production of antimicrobial compounds in response to biotic stress [52]. The members of OGBa produced antimicrobial compounds such as hydrogen cyanide (HCN) and cyclic lipopeptides such as surfactin used to inhibit the growth of pathogenic microbes [53,54]. The interactions of biocontrol agents with plant roots enhance plant resistance against some competing microbes including pathogenic bacteria, fungi and viruses. This phenomenon is termed as induced systemic resistance (ISR) [6,55].
The members of OGBa were proven to provide advantages to the agricultural sector by contributing to plant pathogen disease suppression. In plant disease management, the members of OGBa acted as plant growth-promoting bacteria (PGPB) that aid in the development of plants and reduce the proliferation of plant pathogens (Table 2). The secretion of antimicrobial compounds such as surfactin from PGPB was suggested to trigger the pathways of ISR which contributed to the suppressive effect of plant immunity [56,57]. Surfactin was determined to act as elicitors of plant immunity and enhance resistance towards further pathogenesis in plants [47]. In the lettuce rhizosphere, increased production of surfactin by B. velezensis FZB42 in the axenic system was suggested to contribute to the disease suppression towards Rhizoctonia solani infection [53]. Similarly, the treatment using B. velezensis FZB42 in tobacco plants was suggested improve ISR and enhance plant height and fresh weight, while lowering the disease severity rating of the tobacco mosaic virus (TMV) [58].
Bacterial species from the OGBa are used in bioformulations. For instance, the bacterial strain B. velezensis FZB42 had been established as a model strain for plant growth promotion and as a biocontrol agent [55]. In 2019, tomato seeds coated with gum arabic as adhesive along with liquid bioformulations containing B. velezensis FZB42 showed great inhibitory effects against Fusarium solani infections under in vitro conditions. Increments in germination percentage and germination rate as compared with the control were also reported [81].
To date, there are a few bioformulations containing bacterial species from the OGBa available on the market (Table 3), such as SERENADE® (Bayer Crop Science, Germany) which contains B. velezensis QST 713 (previously B. subtilis QST 713) and Double Nickel 55TM (Certis Columbia, MD USA) which contains B. velezensis D747 (previously B. amyloliquefaciens D747) [55]. The application of SERENADE® together with Fracture fungicide (CEV, Portugal), which contains BLAD polypeptide, had shown notable success in controlling Botrytis blossom blight disease infection in blueberries [82]. Application of Double Nickel 55TM was found to be effective in controlling white mold in snap beans caused by Sclerotinia sclerotiorum. Double Nickel 55TM, a biofungicide, was approved for organic vegetable production by the National Organic Program and Organic Materials Review Institute [83].
Apart from the aforementioned uses, the members of OGBa have also been applied as biocontrol agents against parasitic nematodes and protist pathogens. In 2008, B. velezensis FZB42 was reported to reduce nematode eggs in roots, juvenile worms in soil and plant galls on tomato [84]. Genomic study revealed that the whole genome of B. velezensis FZB42 encoded a diverse spectrum of different antimicrobial compounds able to suppress harmful nematodes living within the plant rhizosphere [85]. In controlling the protist pathogen, B. velezensis HB-26 (previously B. amyloliquefaciens HB-26) showed promising capability for controlling Plasmodiophora brassicae, a root-infecting protist that causes clubroot disease in brassica species. Many antimicrobial compounds showing specific activities against P. brassicae were found in the genome of B. velezensis HB-26 [86]. Overall, much more focus is still needed to fulfill the understanding of the molecular basis for the ability of members of OGBa to inhibit nematodes and protists beyond in silico genomic studies. Understanding such attributes will help to shed light on the functionalities as well as the biological roles of antimicrobial compounds from OGBa not only for improved plant growth but as biocontrol agents to minimize the proliferation of plant pathogens including viruses, bacteria, fungus, nematodes, and protists.

3.2. Source of Commercial Enzymes

Microbial enzymes such as α-amylase, protease, and lipase have been used in various biotechnological applications including textile applications, feed industry, food industry, and organic synthesis [87,88,89]. The U.S. Food and Drug Administration (FDA) in 1999 reported that enzymes such as α-amylase and protease originating from B. subtilis are Generally Recognized as Safe (GRAS) for use as direct food ingredients [90]. As members of the B. subtilis species complex, OGBa bacteria are a potent bacterial group due to their abilities to produce various types of enzymes including α-amylase, protease, lipase, cellulase, xylanase, pectinase, aminotransferase, barnase, peroxidase, and laccase (Table 4).

3.3. Antimicrobial Compounds Producer

The increment in the global antibiotic-resistant pathogens has led to the exploration of compounds with alternative therapeutic strategies [104]. The members of OGBa were reported to produce antimicrobial compounds used in the suppression of pathogens [45]. The antimicrobial compounds produced by the member of OGBa have been reviewed previously [8,105]. The members of OGBa produced some important antimicrobial compounds (Figure 3), including non-ribosomal peptides (surfactin, fengycin, bacillomycin-D, bacilysin and bacillibactin) and polyketides (bacillaene, macrolactin and difficidin) [6,105].
Non-ribosomal peptides produced by bacteria and fungi contain two or more moieties derived from amino acids [106]. The mode of action of non-ribosomal peptides involves the disruption to the cell membrane and inhibition on the transfer of peptidoglycan precursors to bactoprenol pyrophosphate [107]. In 2019, surfactins from B. velezensis 9D-6 were found to inhibit the in vitro growth of bacteria (B. cereus, C. michiganensis, Pantoea agglomerans, Ralstonia solanacearum, Xanthomonas campestris and Xanthomonas euvesicatoria) and fungi (Alternaria solani, Cochliobolus carbonum, F. oxysporum, F. solani, Gibberella pulicaris, Gibberella zeae, Monilinia fructicola, Pyrenochaeta terrestris and R. solani) pathogens [108]. In another related study, in silico genomic study of B. siamensis JFL15 had gene clusters involved in the biosynthesis of antimicrobial compounds. The LC–MS/MS analysis confirmed the presence of iturin A and bacillomycin F. Both compounds showed strong antifungal activities against Magnapothe grisea, R. solani and Colletotrichum gloeosporioides, as analyzed under in vitro conditions [109]. Moreover, the presence of fengycin, bacilysin, and bacillibactin had also been reported from B. velezensis OSY-S3 that showed inhibition activities against Listeria innocua, Escherichia coli, Penicillium sp., Cladosporium sp., and Staphylococcus aureus [110].
Polyketides are biopolymers of acetate and other short carboxylates that are biosynthesized by polyketide synthases, a natural metabolite produced by microorganisms and plants which possess various antifungal and antibacterial activities [111,112]. Since the discovery of polyketides (e.g., streptomycin in 1950), the exploration of new polyketides has assisted pharmaceutical companies in isolating new antibiotic-producing strains as the main sources of antibiotics [113]. Antibacterial polyketides including bacillaene, macrolactin and difficidin were reported from B. velezensis OSY-GA1 [109]. Moreover, B. velezensis YJ11-1-4 isolated from doenjang exhibited good antimicrobial activities against bacterial (B. cereus, E. coli, Listeria monocytogenes and S. aureus) and fungal (Aspergillus flavus subsp. flavus) foodborne pathogens. Genomic analysis reveals the presence of antibiotic biosynthesis operons including bacillaene, macrolactin and difficidin in the genome of B. velezensis OSY-GA1 [114]. Additionally, four new glycosylated macrolactin compounds, namely macrolactins O, P, Q and R, had been isolated from the liquid cultures of B. velezensis AH159-1. These compounds inhibited S. aureus peptide deformylase and also showed antibacterial activities against E. coli and S. aureus [115].

3.4. Potential as Probiotics

Probiotics are live microbial feed supplements that benefit the host animal by improving the microbial balance. Probiotics have become increasingly popular due to continuously expanding scientific evidence pointing to their beneficial effects on both humans and animals [116]. Within the OGBa, some B. velezensis strains are reported to display probiotic potential and have been applied as probiotics for animals [117]. For instance, B. velezensis H57 (previously B. amyloliquefaciens H57) isolated from lucerne was first investigated in the research to prevent fungal spoilage of hay [118]. Because it is an endospore-forming bacterium able to produce antimicrobial compounds, B. velezensis H57 was commercialized as a spoilage control agent under the product name HayRite™ (Biocare and BASF, Australia). Interestingly, sheep and cattle fed on HayRite™ showed improvements in digestibility and nitrogen retention leading to increased weight gain [118]. Genomically, the potential of B. velezensis H57 to synthesize antimicrobial compounds including surfactin (srfABCD), iturin (ituABCD), bacillomycin D (bmyABC), fengycin (fenABCDE), macrolactin (mlnABCDEFGHI), difficidin (dfnABCDEFGHIJ) and bacillaene (baeEDLMNJRS) were suggested to facilitate the probiotic effects of B. velezensis H57 [27]. In another related study, B. velezensis FTC01 manifested itself as a probiotic [119]. Genes coding for hydrolases (peptidases, phytases and glycosidases) that can improve feed digestion and prevent intestinal disorders are present in the genome of B. velezensis FTC01. Additionally, peptidylprolyl isomerase (prsA) gene (a gene that is involved in bacterial adhesion and signaling of biofilm formation in the host gut) was also found. Moreover, in silico genome analysis of B. velezensis FTC01 proved the presence of gene clusters involved in the synthesis of antimicrobial peptides. Similarly, gene clusters involved in the synthesis of antimicrobial peptides were also found in the genome of B. velezensis JT3-1, a probiotic strain isolated from faeces of the domestic yak [21]. The antimicrobial activity of B. velezensis JT3-1 was confirmed using an antimicrobial assay. Strain JT3-1 manifested strong antagonistic activities against various intestinal pathogenic flora including L. monocytogenes, S. aureus, E. coli, Salmonella typhimurium, Mannheimia haemolytica, Staphylococcus hominis, Clostridium perfringens and Mycoplasma bovis.
B. velezensis B-1895 (previously B. amyloliquefaciens B-1895) has been commercially used as a probiotic in the fish industry, particularly for Alburnus leobergi [120,121]. Its probiotic potential was proven thought the Ames test (reported as non-mutagenic) and antimicrobial activities (against Streptococcus intermedius and Porphyromonas gingivalis). Moreover, the endospores of B. velezensis B-1895 were found tolerant to 0.3% (w/v) bile salts and survived incubation for 4 h in MRS broth at pH 2.0–3.0. Overall, the results suggested the potential of B. velezensis B-1895 as a fish probiotic [122]. In another related study, B. velezensis JW also manifested itself as a fish probiotic [123]. Strain JW showed antibacterial activities against a broad range of bacterial fish pathogens (Aeromonas hydrophila, Aeromonas salmonicida, Lactococcus garvieae, Streptococcus agalactiae and Vibrio parahemolyticus). Dietary administration of B. velezensis JW induced an immune response in Carassius auratus. The immune-related genes in C. auratus such as interferon gamma gene (IFN- γ), tumor necrosis factor-α (TNF-α), interleukin-1 (IL-1), interleukin-4 (IL-4) and interleukin-10 (IL-10) were found to be upregulated by B. velezensis JW-supplemented diets. It is noteworthy that C. auratus fed with B. velezensis JW-supplemented diets showed improvements in survival rate after A. hydrophila infection. This was supported genomically by the presence of antimicrobial gene clusters in the genome of B. velezensis JW [122]. Moreover, a potential probiotic effect of B. velezensis V4 on the growth performance of Oncorhynchus mykiss had also been investigated [124]. Cell-free supernatant of B. velezensis V4 with anti-A. salmonicida was shown to contain antimicrobial compounds including iturin, macrolactin and difficidin. The mortality rate of O. mykiss was reduced by 27% and the weight gain ratio was increased by 71% through the 1% (v/w) addition of B. velezensis V4. Overall, the findings demonstrated that B. velezensis V4 was an effective probiotic in O. mykiss.
The commercialization of B. amyloliquefaciens as a probiotic in aquaculture is not as common compared to its agricultural applications (Table 3). Ecobiol® Soluble Plus, is one of the commercial probiotic products reported as containing B. amyloliquefaciens at a concentration of 109 CFU/g, specifically formulated for applications in poultry and swine, as well as in aquaculture. There was research conducted on the commercial probiotic Ecobiol® Soluble to observe its positive effects on the biofloc culture of Litopenaeus vannamei and its benefits on water quality, growth performance and the immune system of shrimps. Three doses of probiotic (9.48 × 104, 1.90 × 105 and 3.79 × 105 CFU/g) were applied to the culture water for 42 days. At the end of the trial, there was no significant improvement in the water quality. However, it showed notable changes in the immune system of the shrimp. As compared to the control treatment, there was an increase in the total protein concentration and granular hemocytes, and a decrease in the cell number with apoptosis in the hemolymph in all treatments. Therefore, other than being mixed with feed, B. amyloliquefaciens in the commercial probiotic Ecobiol® Soluble Plus could also be applied directly to the culture system; this research proved it provided better resistance to shrimps against the outbreak of pathogens in shrimp biofloc systems [125].
There is much ongoing research on the development and formulations of bacterial strains belonging to the OGBa as potential probiotics for commercialization purposes in the aquaculture industry. Most of the studies have emphasized probiotic feed formulations, feeding trials on a small scale before moving to field trials. For instance, dietary inclusion of B. amyloliquefaciens at 106 CFU/g fed to zebra fish improved the expression levels of metabolism-related genes, enzyme activities and oxidative stress-related genes in the fish liver as well as enhanced their immune resistance against pathogenic A. hydrophila and S. agalactiae. In addition, the strain of B. amyloliquefaciens used in this study was able to express recombinant xylanase, an important enzyme that aided in better feed digestibility and efficiency [126]. In another related study, the administration of B. amyloliquefaciens (1 × 109 CFU/g), together with Spirulina platensis in formulated diet for tilapia, improved growth performance and feed utilization after a 60 day feeding trial. The mRNA level of the TNF-α gene and the transcription of SOD were considerably higher in tilapia fed with dietary B. amyloliquefaciens and S. platensis compared to the control group [127]. Moreover, B. amyloliquefaciens at a concentration of 106 CFU/mL provided significant protection to juvenile blue swimming crabs, Portunus pelagicus, when challenged with Vibrio harveyi in in vivo trials [128]. Nevertheless, further studies are necessary, mainly on probiotic formulation along with larger field trials, to strengthen the outcomes in order to be able to commercialize bacterial strains belonging to the OGBa for aquaculture use.
In vivo and field trials are critical in probiotic development. Occasionally, there were negative outcomes in in vivo studies which were carried out based upon the positive results acquired from the preliminary in vitro assays, which indicated the possibility of negative correlations between trials in vitro and in vivo. Hence, it is crucial to understand and to optimize various conditions in in vivo studies or field trials including the probiotic formulation which may affect the survival, colonization, proliferation, and interaction of the probiotic with the host in a certain environment [129].

3.5. Potential as Bioremediation Agents

The use of microorganisms as bioremediation agents has become a burgeoning trend [130]. To date, most research focused on the plant growth-promoting activity and antimicrobial compounds of OGBa is as described above. Interestingly, in 2019, B. amyloliquefaciens YP6 was reported to exhibit both plant growth-promoting activity and broad-spectrum organophosphorus pesticide (OP) removal [131]. In silico genome analysis of B. amyloliquefaciens YP6 found it to contain a variety of promising genes, including phosphorus solubilizing and OP-degrading related genes (phoD, phoA, phrC, phoE, ycsE, bcrC and yvaK), indole-3-acetic acid synthesis related genes (amhX, cgeE and epsM), and siderophores synthesis related genes (entB, menF, entC and entA). The results hinted at the potential application of B. amyloliquefaciens YP6 in agricultural and environmental remediations. Overall, much more focus is still needed to understand the OP-degrading related genes beyond in silico genome analysis. Therefore, it is necessary to conduct further studies to determine the in vitro functional genomics and the OP-degrading enzyme activities of the members of OGBa. Understanding such attributes will help to shed light on the applicability of the OGBa in OPs degradation and in the bioremediation processes as a whole.

4. Concluding Remark and Future Perspectives

In conclusion, the progress of the research on the biotechnological applications of bacterial species that belong to OGBa is remarkable. The bacteria are important not only industrially, but also environmentally. A plethora of studies have addressed the abilities of the members of OGBa as plant growth-promoters, biocontrol agents, probiotics, bioremediation agents as well as producers of commercial enzymes and antibiotics. Moreover, the use of the bacteria in optimized bioformulations as well as the demonstration of the great success of the commercialized products give us hope towards more sustainable agricultural and aquacultural industries. Owing to the listed biotechnological applications and potentials, more research should be done focusing on the integration of system biology data derived from genomics, phenomics, proteomics, metabolomics and fluxomic analyses in order to expand our basic understanding on the versatility of the members of OGBa. Enabling the prediction of cellular functions and metabolites produced by the members of this operational group could provide fundamental knowledge towards the enhancement of the applications of their potentials in biotechnology and bioprocessing for the benefit of all.

Supplementary Materials

The following are available online at https://www.mdpi.com/2076-2607/9/3/614/s1: Table S1. Bacterial strains from the operational group Bacillus amyloliquefaciens.

Author Contributions

Conceptualization, M.S.N. and S.S.; writing—original draft preparation, M.S.N.; writing—review and editing, M.S.N., R.S.R.Y., M.M.A.-a.B., S.M.Y., M.K., S.A.A. and S.S.; visualization, M.S.N., R.S.R.Y., M.M.A.-a.B., S.M.Y., M.K., S.A.A. and S.S.; supervision, S.S.; project administration, S.S.; funding acquisition, S.S. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the UPM-Putra Graduate Initiative (GP-IPS/2018/9601400). M.S.N., R.S.R.Y. and M.M.A.B. were sponsored by Graduate Research Fellowships (GRF) from Universiti Putra Malaysia.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Microorganisms 09 00614 g001 550
Figure 1. Neighbor-joining phylogenetic tree based on complete rpoB nucleotide sequences of bacterial species under the B. subtilis species complex. Evolutionary analyses were conducted using the MEGAX software [15]. The optimal tree with the sum of branch length = 0.66533958 is shown. The evolutionary distances were computed using the p-distance method. Bootstrap values, based on 1000 repetitions, are indicated at the branch points. The analysis involved 19 nucleotide sequences. There were 3534 positions in the final dataset. Bar, 0.02 substitutions per nucleotide position. Bacillus cereus ATTC 14579T was used as the outgroup.
Figure 1. Neighbor-joining phylogenetic tree based on complete rpoB nucleotide sequences of bacterial species under the B. subtilis species complex. Evolutionary analyses were conducted using the MEGAX software [15]. The optimal tree with the sum of branch length = 0.66533958 is shown. The evolutionary distances were computed using the p-distance method. Bootstrap values, based on 1000 repetitions, are indicated at the branch points. The analysis involved 19 nucleotide sequences. There were 3534 positions in the final dataset. Bar, 0.02 substitutions per nucleotide position. Bacillus cereus ATTC 14579T was used as the outgroup.
Microorganisms 09 00614 g001
Microorganisms 09 00614 g002 550
Figure 2. The biological control interactions. The illustration depicts the interactions between biocontrol agents, plant pathogens, and plants. The biocontrol agent colonized the plant root surface and produced antimicrobial compounds such as surfactin. In the plant rhizosphere, antibiosis and nutrient competition interaction suppressed the growth of pathogens. Due to the production of antimicrobial compounds and in the simultaneous presence of pathogens, the induced systemic resistance (ISR) is enhanced. Thus, this mediated the defense response of the plant towards pathogens and consequently improved plant growth and the defense mechanism against pathogens.
Figure 2. The biological control interactions. The illustration depicts the interactions between biocontrol agents, plant pathogens, and plants. The biocontrol agent colonized the plant root surface and produced antimicrobial compounds such as surfactin. In the plant rhizosphere, antibiosis and nutrient competition interaction suppressed the growth of pathogens. Due to the production of antimicrobial compounds and in the simultaneous presence of pathogens, the induced systemic resistance (ISR) is enhanced. Thus, this mediated the defense response of the plant towards pathogens and consequently improved plant growth and the defense mechanism against pathogens.
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Figure 3. Antimicrobial compounds produced by members of the operational group Bacillus amyloliquefaciens.
Figure 3. Antimicrobial compounds produced by members of the operational group Bacillus amyloliquefaciens.
Microorganisms 09 00614 g003
Table
Table 1. Characterizations of bacterial species under the operational group Bacillus amyloliquefaciens.
Table 1. Characterizations of bacterial species under the operational group Bacillus amyloliquefaciens.
CharacterizationB. amyloliquefaciensB. siamensisB. velezensisB. nakamurai
Type StrainDSM 7T / ATCC 23350T / FTKCTC 13613T / PD-A10T / BCC 22614TNRRL B-23189T / CR-502T / CECT 5686T / LMG 22478TNRRL B-41091T / CCUG 68786T
Isolation SourceSoil and industrial α-amylase fermentationsSalted crab (poo-khem) in ThailandBrackish water sample from the river Velez at Torredelmar in Ma’laga,
southern Spain		Soil in Tierra del Fuego, Argentina
Size0.7–0.9 × 1.8–3.0 µm0.3–0.6 × 1.5–3.5 µm0.5 × 1.5–3.5 µm0.74–0.93 × 1.39–2.04 µm
EndosporeOval spores are central or paracentral in unswollen sporangia Ellipsoidal spores are central or sub-terminal positions in swollen sporangiaEllipsoidal spores are paracentral or sub-terminal positions in
unswollen sporangia		Ellipsoidal spores are central in unswollen sporangia
G + C Content (mol %)44.641.446.1–46.443.8
Growth TemperatureOptimal growth temperature is 30–40 °C. No growth occurs below 15 °C or above 50 °C.Optimal growth temperature is 37 °C. Growth occurs at 4 °C and 55 °C. Grow within
the temperature range of 15–45 °C		Grow within
the temperature range of 17–50 °C, with an optimum of 37 °C
NaCl Resistance (w/v)Growth occurs with 0–10% NaClGrowth occurs with 0–14% NaClGrowth occurs with 0–12% NaClGrowth occurs with 0–9% NaCl
Substrate
Utilization		Tyrosine---+
Citrate+--+
Fermentation (acid)Lactose+++-
Trehalose+-++
Reference[1][16][17][18]
Note: All the bacterial species are able to metabolize casein, gelatin, starch, fructose, cellobiose, glucose, glycerol, maltose, mannitol, raffinose, salicin and sucrose. Symbol: +, positive result; -, negative result.
Table
Table 2. Plant pathogen suppression by members of the operational group Bacillus amyloliquefaciens in various plant species.
Table 2. Plant pathogen suppression by members of the operational group Bacillus amyloliquefaciens in various plant species.
PGPB StrainDisease and PathogenPlant SpeciesReference
B. siamensis KCTC 13613R. solani
Botrytis cinerea
Micrococcus luteus		Arabidopsis thaliana[59]
B. velezensis 83Anthracnose diseaseZea mays
A. thaliana		[20]
B. velezensis 1B-23Clavibacter michiganensis subsp. michiganensisSolanum lycopersicum[60]
B. velezensis B25Fusarium verticillioidesZ. mays[61]
B. velezensis BTLK6AMagnaporthe oryzae TriticumTriticum aestivum[62]
B. velezensis BTS 4
B. velezensis CC09Powdery mildew diseaseT. aestivum[28]
B. velezensis CGMCC 11640Botryosphaeria dothideaCarya cathayensis[63]
B. velezensis Co1-6Verticillium dahliae
R. solani
Fusarium culmorum
Ralstonia solanacearum		Matricaria chamomilla[64]
B. velezensis GB1Valsa maliMalus domestica[65]
B. velezensis GH1-13Fusarium fujikuroi
R. solani
Xanthmonas oryzae		Oryza sativa[49]
B. velezensis GQJK49F. solaniLycium barbarum L.[66]
B. velezensis GYL4Anthracnose diseaseCucumis sativus L. cv. Chunsim[67]
B. velezensis J-5B. cinereaS. lycopersicum[68]
B. velezensis JKM. oryzaeO. sativa[69]
B. velezensis L-1Botryosphaeria berengerianaPyrus communis[70]
B. velezensis LM2303Fusarium graminearumT. aestivum[71]
B. velezensis M27Sclerotinia sclerotiorumLactuca sativa L.[72]
B. velezensis NJAU-Z9Fusarium oxysporum f. sp. niveum
Ralstonia solanacearum		Capsicum annuum L.[73]
B. velezensis NJN-6F. oxysporum f. sp. cubenseMusa sp.[74]
B. velezensis OEE1F. solaniOlea europaea L.[75]
B. velezensis P42Bacterial wilt and early blight diseasesS. lycopersicum[76]
B. velezensis PG12Apple ring rot diseaseMalus domestica[24]
B. velezensis TrigoCor1448Fusarium head blight diseaseT. aestivum[77]
B. velezensis UCMB5113Alternaria brassicae
B. cinerea
Leptosphaeria maculans
Verticillium longisporum		Brassica napus[78]
B. velezensis XK-4-1Verticillium wilt diseaseGossypium sp.[79]
B. velezensis ZF2Corynespora leaf spot diseasesC. sativus[80]
Table
Table 3. Some commercial products containing the members of the operational group Bacillus amyloliquefaciens available on the market.
Table 3. Some commercial products containing the members of the operational group Bacillus amyloliquefaciens available on the market.
Bacterial StrainCommercial ProductCompanyDescription
B. velezensis QST 713
(previously B. subtilis QST 713)		SERENADE MaxBayer Crop Science, previously AgraQuestEPA-registered biofungicide. Controls and suppresses fungal pathogens on foliage and in the soil
SERENADE SOIL®Bayer Crop Science, previously AgraQuestEPA-registered biofungicide for food crops
CEASE®BioWorks, Inc., Victor, New York, U.S.A.Aqueous suspension biofungicide for leafy and fruiting vegetables, herbs and spices, and ornamentals
B. velezensis FZB42
(previously B. amyloliquefaciens FZB42)		RhizoVital® 42ABiTEP GmbH, Berlin, GermanyBiofertilizer, plant-growth-promoting activity, provides protection against various soil-borne diseases
FZB24® TBABiTEP GmbH, Berlin, Ger-manyPlant growth-promoting agent for plant strengthening
Taegro®Syngenta, Basel, previously Novozyme, Davis, California, and Earth BiosciencesEPA-registered biofungicide for use in North America
B. velezensis GB03
(previously B. subtilis GB03)
Kodiak™Bayer Crop Science, North Carolina, NCEPA-registered biological seed treatment fungicide with demonstrable PGR activity. Efficient in cotton, beans, and vegetables
CompanionGrowth Products Ltd., White Plains, NYEPA-registered biofungicide that prevents and controls plant diseases
B. velezensis D747
(previously B. amyloliquefaciens D747)		Double Nickel 55™Certis Columbia, MD, U.S.A.EPA-registered biofungicide for control or suppression of fungal and bacterial plant
Amylo-X®Certis Columbia, MD USA/Intrachem Bio Italia SpABiocontrol of Botrytis and other fungal diseases of grapes, strawberries, and vegetables, and bacterial diseases, such as fire blight in pome fruit and PSA in kiwi fruit
Table
Table 4. Various types of enzymes produced by members of the operational group Bacillus amyloliquefaciens.
Table 4. Various types of enzymes produced by members of the operational group Bacillus amyloliquefaciens.
Bacterial SpeciesEnzymesReference
B. amyloliquefaciens KCP2α-amylase and protease[91]
B. amyloliquefaciens NRRL 942α-amylase[92]
B. siamensis JJC33Mα-amylase[93]
B. velezensis 157α-amylase, cellulase, xylanase and pectinase[94]
B. velezensis 275Cellulase, xylanase, peroxidase, and laccase[95]
B. velezensis AP194Pectinase[96]
B. velezensis AP214Pectinase[96]
B. velezensis GZBLaccase[97]
B. velezensis JJ-D34α-amylase, protease and cellulase[98]
B. velezensis Jxnuwx-1Protease[99]
B. velezensis SB1216Barnase[100]
B. velezensis SPZ1Lipase[101]
B. velezensis SYBC H47Aminotransferase[102]
B. velezensis ZL918α-amylase[103]
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Ngalimat, M.S.; Yahaya, R.S.R.; Baharudin, M.M.A.-a.; Yaminudin, S.M.; Karim, M.; Ahmad, S.A.; Sabri, S. A Review on the Biotechnological Applications of the Operational Group Bacillus amyloliquefaciens. Microorganisms 2021, 9, 614. https://doi.org/10.3390/microorganisms9030614

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Ngalimat MS, Yahaya RSR, Baharudin MMA-a, Yaminudin SM, Karim M, Ahmad SA, Sabri S. A Review on the Biotechnological Applications of the Operational Group Bacillus amyloliquefaciens. Microorganisms. 2021; 9(3):614. https://doi.org/10.3390/microorganisms9030614

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Ngalimat, Mohamad Syazwan, Radin Shafierul Radin Yahaya, Mohamad Malik Al-adil Baharudin, Syafiqah Mohd. Yaminudin, Murni Karim, Siti Aqlima Ahmad, and Suriana Sabri. 2021. "A Review on the Biotechnological Applications of the Operational Group Bacillus amyloliquefaciens" Microorganisms 9, no. 3: 614. https://doi.org/10.3390/microorganisms9030614

APA Style

Ngalimat, M. S., Yahaya, R. S. R., Baharudin, M. M. A. -a., Yaminudin, S. M., Karim, M., Ahmad, S. A., & Sabri, S. (2021). A Review on the Biotechnological Applications of the Operational Group Bacillus amyloliquefaciens. Microorganisms, 9(3), 614. https://doi.org/10.3390/microorganisms9030614

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