Research Article | Open Access
Sowmiya Sattanathan1, Vidya Sriraman1, J. Jemina1, M. Ranjani2, Anwesha Anurupa1, Mohandass Ramya1 and Pasupathi Rathinasabapathi1
1Department of Genetic engineering, SRM Institute of Science and Technology, Kattankulathur, Chengalpattu district, Tamil Nadu, India.
2SRM-DBT platform, SRM Institute of Science and Technology, Kattankulathur, Chengalpattu district, Tamil Nadu, India.
Article Number: 8958 | © The Author(s). 2024
J Pure Appl Microbiol. 2024;18(1):467-475. https://doi.org/10.22207/JPAM.18.1.30
Received: 01 September 2023 | Accepted: 17 January 2024 | Published online: 28 February 2024
Issue online: March 2024
Abstract

Panchagavya has traditionally been used in Indian Ayurvedic practices because of its pro-agricultural and medicinal properties. This study presents the draft genome of a new Brevibacillus brevis S1-3 strain isolated from the fermented product Panchagavya. Through whole-genome sequencing, we determined that the genome of B. brevis S1-3 was 6,348,716 base pairs with a GC content of 54.3%. Genome assembly revealed the presence of 6107 protein-coding genes, 186 tRNA genes, and 13 rRNA genes. Genome annotation and analysis identified the genes involved in metabolism and other cellular processes. We also predicted the presence of several gene clusters associated with plant growth promotion, including indole acetic acid (IAA), gibberellic acid, ammonia, and nitrogen. Our study also revealed the genes responsible for the production of secondary metabolites that displayed a significant correlation with antimicrobial activity. Our results provide new insights into the genomic basis of the plant growth-promoting abilities of B. brevis and pave the way for further research in this field.

Keywords

Brevibacillus brevis, Draft Genome Sequencing, Panchagavya, Plant Growth Promotion, Secondary Metabolite, Ayurvedic Practices

Introduction

Brevibacillus brevis is a gram-positive, motile, rod-shaped, aerobic spore-forming bacterium known to be present in various environmental conditions, including soil and the animal guts.1,2 This bacterium has been shown to possess antimicrobial activity against soil-borne pathogens such as Phytophthora nicotianae and Ralstonia solanacearum,3,4 making it a potential control agent against plant pathogens. Additionally, B. brevis produces a variety of secondary metabolites, such as tyrocidine, grastin, and adenine, which are responsible for its antimicrobial activity.5-7 Brevibacillus brevis has also been studied to identify its role and interaction with plants and has been found to confer disease resistance against fungal agents in plants like tomatoes,8 grapes,9 pigeon pea,10 tea,11 etc. Furthermore, B. brevis has been identified as a plant-growth-promoting rhizobacterium (PGPR),12-14 which can act as a biofertilizer, increasing crop yield and soil fertility, while reducing the need for chemical fertilizers.15

Several studies have reported draft genome sequences of several strains of B. brevis, including NBRC 100599,16 B. brevis X23,14 and B. brevis strain FJAT-0809-GLX.13 These genome sequences typically range in size from 6Mb and contain more than 5600 protein-coding genes. However, these previously published genomes are yet to undergo functional annotation to identify the genes responsible for the biosynthesis of secondary metabolites or plant growth regulators.

In the field of plant-microbe interactions, biocontrol is a dynamic strategy that uses beneficial microbes to control plant pathogens. The biocontrol arsenal includes systemic resistance, antimicrobial compounds, competitive exclusion, and nutrient enhancement.17 The success of biocontrol depends on factors such as compatibility, adaptability, persistence, and specificity, which collectively determine its effectiveness. Integrating these methods with other pest management approaches is essential for sustainable agriculture.18 However, achieving a delicate balance between inducing resistance without harmful effects and addressing practical application challenges remains a complex task.

Recent advancements highlight the crucial roles of plant-associated microorganisms in maintaining plant health and ecological balance. Utilizing beneficial microbes is a promising approach for disease mitigation and improved crop yields.19 Genomic and proteomic analyses of microbial genomes provide insights into the molecular intricacies of these interactions, which are critical for refining control measures. While previous research focused on the rhizosphere, the phyllosphere, which includes aboveground plant parts, is less explored.20

B. brevis is recognized as a noteworthy inhabitant of the rhizosphere, showcasing remarkable biocontrol capabilities through its interactions with plants. In this study, we isolated a new strain of Brevibacillus brevis S1-3 from Panchagavya, a fermented product traditionally used in Indian Ayurvedic practices that is composed of five cow products, including clarified butter, curd, milk, urine, and fermenting dung.21,22 Through genome sequencing and functional annotation, we characterized the genome of B. brevis S1-3, providing new insights into the genomic basis of the biosynthesis of secondary metabolites and plant growth regulators in this strain.

Materials and Methods

Isolation and Molecular Identification
The Panchagavya used in this study were obtained from a commercial market in Chennai, India. After serial dilutions, the bacterial species present in Panchagavya were grown in Luria-Bertani medium at 37°C. Distinct colonies were then selected and cultured separately before storage at -20°C. Genomic DNA was extracted from the selected bacteria using the QIAamp DNA Microbiome Kit (Qiagen India Pvt. Ltd., India), according to the manufacturer’s instructions. The quality and quantity of the extracted bacterial genomic DNA were analyzed using agarose gel electrophoresis and Nanodrop (Tecan-Infinite 200 PRO, Switzerland). PCR was performed using the 16s rDNA universal primers 27F (5′-AGAGTTTGATCCTGGCTCAG-3′) and 1492R (5′-TACGGTTACCTTGTTACGACTT-3′).23,24 The amplified PCR product was purified (using a Qiagen PCR product purification kit) and sequenced using the Sanger DNA sequencing method (Applied Biosystems Genetic Analyzer, Saint Aubin, France). The resulting 16s rDNA sequences were compared to those in the NCBI database using the Basic Local Alignment Search Tool (BLAST). The bacterial species were identified based on sequence similarity, and a phylogenetic tree was constructed using the MEGAX software. Evolutionary distances were inferred using the neighbour-joining method.25-27

Genome Sequencing and Annotation
Paired-end sequencing libraries were prepared using a Nextera XT DNA Library Preparation Kit (Illumina). The final library was analyzed using a Bioanalyzer 2100 (Agilent Technologies, USA) with a high-sensitivity DNA kit according to the manufacturer’s instructions. The paired-end Illumina library was sequenced using 2 x 150 bp chemistry on a NextSeq-500 sequencer. Quality control of the raw reads was performed using FastQC v.0.11.5,28-30 and the low-quality reads were filtered. The Cutadapt tool was used to remove adapter regions from sequencing reads. High-quality reads obtained from Illumina NextSeq-500 were assembled into scaffolds using SPAdes (version 3.7.1) with default parameters.31-33 The quality of the assembled genome was analyzed using QUAST.

Genome assembly was annotated using Prokka v.2.1.1 and Rapid Annotation using Subsystems Technology (RAST) server v.2.0. Secondary metabolite gene clusters were identified using the antiSMASH version 5. The various biological features of the annotated genome were analyzed using RAST. Antimicrobial resistance genes and other protein functions were identified using PATRIC genome analysis server.34-36

RESULTS AND DISCUSSION

Isolation of culture and phylogenetic analysis
We isolated various bacterial strains and evaluated their antimicrobial activity. Antibacterial activity was examined using broth microdilution assays against Streptococcus aureus (NCBI_CP00253), E. coli (NCBI_U00096), and Vibrio cholerae (NCBI_CP043554). One of the bacterial isolates that exhibited antimicrobial activity was selected for this study.

We isolated several bacterial strains from Panchagavya and assessed their antimicrobial potential. The antibacterial activity of these strains was evaluated using broth microdilution assays against three target pathogens: Streptococcus aureus, E. coli, and Vibrio cholerae (data not shown). One strain demonstrated notable antimicrobial activity among the bacterial isolates tested, prompting its selection for further investigation. The selected bacterial isolate was identified by 16s rDNA sequencing; and showed high similarity to Brevibacillus brevis (NR_041524). The 16s rDNA gene sequence of Brevibacillus brevis S1-3 was used to construct a phylogenetic tree (Figure 1), which revealed that the isolate was closely related to B. brevis NBRC and B. choshinensis with 99.2% and 98.38% sequence similarity, respectively. Other closely related species included B. agri and B. agri DSM 6348T, with 97.5% and 97.3% sequence similarity, respectively. The bacterial isolate identified in this study was named Brevibacillus brevis S1-3. The efficiency of Brevibacillus brevis as a plant growth-promoting rhizobacterium (PGPR) has been determined through studies evaluating its application in fostering plant growth.2 Through the examination of several plant growth-promoting (PGP) features, such as ammonia synthesis, and the generation of phytohormones, such as indole-3-acetic acid (IAA), Brevibacillus brevis’ efficiency in promoting plant growth, evaluations of seed germination, and several plant growth metrics have also been made.37 Bacillus brevis has been found to provide a multi-pronged defense against fungal and microbial pathogens by means of extracellular secretion of gramicidin S, gramicidin A, and a biosurfactant, thereby functioning as a biological control agent and aiding plant growth, apart from the production of PGPs.38

Figure 1. Phylogenetic analysis of 16S rDNA sequence of Brevibacillus brevis S1-3 strain using neighbor-joining method. Pseudomonas aeruginosa was used as an outgroup

Whole Genome Sequencing of B. brevis S1-3
Genome sequencing of B. brevis S1-3 was performed using the Illumina NextSeq-500 platform. A total of 1,602,833 paired-end reads of 101bp were generated, with an average GC content of 54.3% (Table 1). These reads were assembled using SPAdes software, resulting in a draft genome of 5,845,263 bp in size, comprising 187 contigs (N50 – 88,031 bp) and 20 scaffolds (N50 – 678,417 bp). The genome contained 6,107 protein-coding sequences (CDS), 186 tRNA genes, and 13 rRNA operons (16S-23S-5S rRNA)
(Figure 2). Genome annotation was performed using the Prokka and RAST servers, which revealed that out of the total of 2,616 proteins, 2,492 were annotated as ‘hypothetical’ while the remaining proteins had non-hypothetical functions. The annotation included 5,259 proteins with functional assignments, including 1,592 proteins with Enzyme Commission numbers, 1,355 with Gene Ontology (GO) assignments, and 1,201 proteins mapped to KEGG pathways. The quality of the genome assembly was evaluated using QUAST and showed that the genome assembly of B. brevis S1-3 was of high quality.

Table (1):
General genome features of Brevibacilus brevis S1-3 strain plant growth promoting bacteria isolated from Panchagavya.

Features
S1-3 chromosome
Genome size
6,348,716
G + C (%)
55.2
Predicted CDS
5800
rRNAs
13
tRNAs
186

G+C (%): guanine and cytosine content; CDS: protein-coding genes; rRNAs: ribosomal RNA; tRNAs: transfer RNA

Figure 2. The chromosome organization of Brevibacillus brevis S1-3, a plant growth-promoting bacteria isolated from Panchagavya. Circularized DNA plotter diagram of the chromosome of B. brevis, oriented from the origin; the outer light blue circle designates the genome base positions, and the outer blue circles depict predicted 5800 CDSs on both forward and reverse strands. The purple and green combination circle states important chromosomal core structures with DNA elements like tRNA, GC skew+, GC skew-, and rRNA contig. The inner black circle denotes GC content.

Genome annotation
Genome annotation of B. brevis S1-3 assigned many genes to cellular processes related to metabolism, such as membrane transport, dormancy and sporulation, cellular signalling and regulation, cell wall synthesis, and capsule formation. Additionally, many genes were correlated with biosynthesis of a diverse group of macromolecules, such as amino acids, carbohydrates, cofactors, vitamins, prosthetic groups, and pigments (Table 2). A similar study conducted on Brevibacillus brevis LABIM17 proved its antimicrobial property against plant pathogens by brevis through the production of octapeptin and, auranticin.39

Table (2):
Annotation of genes involved in metabolism and other cellular processes of Brevibacillus brevis S1-3 plant growth-promoting bacteria isolated from Panchagavya

Genes function Compounds No. of genes
Genes related to metabolism Fatty acids, lipids and isoprenoids 215
Amino acids and derivatives 625
Sulphur 57
Carbohydrates 560
Cofactors, vitamins, prosthetic groups and pigments 381
Aromatic compounds 45
DNA 140
Phosphorous 85
Iron 29
Secondary metabolism 8
Nitrogen 16
Nucleosides and nucleotides 163
Potassium 13
RNA 207
Genes related to cellular processes Cell division and cellular cycle 56
Dormancy and sporulation 141
Cellular wall and capsule formation 145
Photosynthesis 0
Miscellaneous 67
Motility and chemotaxis 118
Regulation and cell signalling 115
Phages, prophages, transposable elements and plasmids 14
Respiration 109
Response to stress 124
Membrane transport 226
Virulence, disease and defence 128

Identification of genes involved in plant growth promotion and secondary metabolite biosynthesis
B. brevis also exhibits PGP traits at high temperatures, making it a valuable inoculant for cotton crops. Previous studies have reported that B. brevis enhances plant growth by increasing the expression of plant growth promoters such as IAA, ammonia, siderophores, cytokinins, and GA3.2,40,41 Analysis of B. brevis S1-3 revealed that the genome contains many genes involved in the biosynthesis of plant growth promoters (PGP) (Table 3). The presence of five structural genes, trpE, trpD, trpC, trpB, and trpA in B. brevis S1-3 predicted the indole acetic acid production through the tryptophan pathway.42 The amoA and amoCAB code ammonia monooxygenase, which is essential for ammonia production. nifD, nifK, and nifH are responsible for metabolism involved in nitrogen fixation. entA, entB, and entC encode 2,3-dihydro-2,3-dihydroxybenzoate synthetase, which is essential for siderophore production.43 Cytokinin production was predicted based on the presence of Tzs genes, which encode cytochrome P450 monooxygenase, the key enzyme for cytokinin production.44 ggs1 and ggs2 initiate the GGDP pathway for primary metabolism of gibberellic acid.45 The presence of these genes in B. brevis S1-3 suggests that this strain has potential applications in agriculture as a biofertilizer and for controlling plant pathogens.

Table (3):
Plant growth promotor (PGP) gene cluster identified in B. brevis S1-3 strain

Plant growth promotor
Genes
IAA (Indole Acetic Acid)
Iaam, Iac, IaaH, IaaL, trpE(G), ipdC
Ammonia and Nitrogen
amoA, amoCAB, nifD, nifK, nifH
Siderophore
Sid, agbB, entB, entC, entA
Cytokines
Tzs, TLRs, PDGFA, PDGFB, PDGFC, PDGFD
GA3
P450-3, P450-4, NPB20, ggs1, ggs2

The gene clusters involved in the biosynthesis of secondary metabolites in B. brevis S1-3 were identified using the antiSMASH 5.1.2 software (Table 4). This analysis revealed 97 genes associated with antibiotic resistance, 47 genes related to drug targets, 79 transporter genes, and 96 virulence factor genes. The genes were classified based on their antimicrobial resistance mechanisms, as determined by various antimicrobial resistance databases.46-49 This study provides a comprehensive understanding of the genomic basis for the plant growth-promoting and secondary metabolite biosynthetic abilities of B. brevis S1-3 and, provides a foundation for future research in this area.

Table (4):
Antimicrobial Resistance Genes from Brevibacillus brevis S1-3

AMR Mechanism
Genes
Antibiotic inactivation enzyme
ANT(6)-I, FosB, PDC family
Antibiotic target in susceptible species
Alr, Ddl, dxr, EF-G, EF-Tu, folA, Dfr, folP, gyrA, gyrB, inhA, fabI, Iso-tRNA, kasA, MurA, rho, rpoB, rpoC, S10p, S12p
Antibiotic target modifying enzyme
Cfr
Efflux pump conferring antibiotic resistance
EmrAB-OMF, EmrAB-TolC, FexA family, MdtABC-OMF, MdtABC-TolC, MexAB-OprM, MexCD-OprJ, MexCD-OprJ system, MexEF-OprN, MexHI-OpmD, MexHI-OpmD system, MexJK-OprM/OpmH, MexVW-OprM, MexXY-OMP, YkkCD
Gene conferring resistance via absence
gidB
Protein altering cell wall charge conferring antibiotic resistance
GdpD, PgsA
Protein modulating permeability to antibiotic
OccD4/OpdT, OccD6/OprQ, OccK8/OprE, OprD family
Regulator modulating expression of antibiotic resistance genes
LiaF, LiaR, LiaS
CONCLUSION

This study isolated and characterized a new strain of Brevibacillus brevis, designated as S1-3, from Panchagavya. The 16s rDNA sequencing and phylogenetic analysis revealed that the isolate was closely related to B. choshinensis and B. agri 5-2. Genome sequencing of B. brevis S1-3 revealed that the genome is of high quality and contains a wide range of genes involved in various cellular processes, including metabolism, cell wall synthesis, and capsule formation. In addition, the genome contains many genes involved in the biosynthesis of plant growth promoters and secondary metabolites. The presence of genes involved in the biosynthesis of indole acetic acid, ammonia, nitrogen fixation, siderophores, cytokinins, and gibberellic acid suggests that this strain has potential applications as a biofertilizer and in controlling plant pathogens. Furthermore, identifying the genes involved in antibiotic resistance, drug targets, transport, and virulence factors may provide insights into the potential biotechnological applications of this strain. The results of this study expand our understanding of the genetic and functional diversity of B. brevis and provide a foundation for future research.

Declarations

ACKNOWLEDGMENTS
None.

CONFLICT OF INTEREST
The authors declare that there is no conflict of interest.

AUTHORS’ CONTRIBUTION
PR and MRam conceptualized the idea. SS, AA and VS isolated and sequenced the genome of Brevibacillus brevis S1-3. JJ and MRan performed Genome annotation. PR, VS and JJ wrote the manuscript. All authors read and approved the final manuscript for publication.

FUNDING
None.

DATA AVAILABILITY
All datasets generated or analyzed during this study are included in the manuscript.

ETHICS STATEMENT
Not applicable.

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