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. 2024 Mar 27:15:1357818.
doi: 10.3389/fmicb.2024.1357818. eCollection 2024.

Genomic insights from Lactiplantibacillus plantarum BRD3A isolated from Atingba, a traditional fermented rice-based beverage and analysis of its potential for probiotic and antimicrobial activity against Methicillin-resistant Staphylococcus aureus

Surmani Huidrom  1   2 , Ng Ngashangva  1 , Joshua Khumlianlal  1   2 , Kongbrailatpam Chandradev Sharma  1 , Pulok Kumar Mukherjee  1 , Sarangthem Indira Devi  1
Affiliations

Genomic insights from Lactiplantibacillus plantarum BRD3A isolated from Atingba, a traditional fermented rice-based beverage and analysis of its potential for probiotic and antimicrobial activity against Methicillin-resistant Staphylococcus aureus

Surmani Huidrom et al. Front Microbiol. .

Abstract

Lactiplantibacillus plantarum BRD3A was isolated from Atingba, a traditional fermented rice-based beverage of Manipur. Its genomic sequence has 13 contigs and its genome size is 3,320,817 bp with a guanine-cytosine (GC) ratio of 44.6%. It comprises 3185 genes including 3112 coding sequences (CDSs), 73 RNAs (including 66 tRNAs and others), and one clustered regularly interspaced short palindromic repeat (CRISPR) array. A comparative and phylogenetic analysis with the Lp. plantarum genome shows that this strain has close similarity with other Lp. plantarum strains and about 99% average nucleotide identity. Functional annotation using evolutionary genealogy of genes-non-supervised orthologous groups (EggNOG) and Kyoto Encyclopedia of Genes and Genomes (KEGG) reveals genes associated with various biological processes such as metabolism, genetic information processing, and transport functions. Furthermore, the strain harbors bacteriocins like plantaricin E, Plantaricin F, and Enterocin X categorized under class IIb by the BAGEL4 database, indicating its potential antimicrobial properties. Additionally, AntiSMASH web server predicted four secondary regions-T3PKS, terpene, cyclic lactone inducer, and ribosomally synthesized and post-translationally modified peptide (RiPP)-suggesting an even higher antimicrobial potential. We validated the antimicrobial activity of Lp. plantarum BRD3A through in vitro experiments in which it exhibited promising bactericidal effects on methicillin-resistant Staphylococcus aureus, inhibiting their biofilm growth. These findings indicate the potential of Lp. plantarum BRD3A to be used as an alternative to conventional antibiotics.

Keywords: Lactobacillus; MRSA; antimicrobial; fermented rice beverages; genome; probiotic; secondary metabolites.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Circular genomic map of Lactiplantibacillus plantarum BRD3A using Proskee View server showing the characteristics features from outside to inner of the circle: CDS, RNA, GC skewness, and GC content are indicated in color code.
Figure 2
Figure 2
Phylogenetic comparisons of Lactiplantibacillus plantarum BRD3A with representative genomes of other reference strains carried out in the TYGS webserver indicate Lp. plantarum WCFS1 was the closest strain. The tree was inferred with FastME 2.1.6.1 from GBDP distances calculated from genome sequences. The branch lengths are scaled in terms of GBDP distance. The numbers above branches are GBDP pseudo-bootstrap support values > 60% from 100 replications.
Figure 3
Figure 3
Heat map of OrthoANI of Lp. plantarum BRD3A compared with closely related Lp. plantarum strains that show 99% similarity with Lp. plantarum WCFS1, Lp. plantarum ST-IlI, and Lp. plantarum ATCC 8014.
Figure 4
Figure 4
(A) EggNOG prediction of Cluster of Orthologous group (COG) functional categories to the proteins BRD3A strain, (B) KEGG orthology (KO) categories of identified protein-coding genes in the Lp. plantarum BRD3A, and (C) OrthoVenn diagram indicates the distribution of common genes (orthologous clusters) among Lp. plantarum STIII, Lp. plantarum JDM1, Lp. plantarum LP3, Lp. plantarum ATCC 8014, and Lp. plantarum BRD3A.
Figure 5
Figure 5
Prophage regions by PHASTER which shows all the regions including the 4 prophage regions in the BRD3A genome which shows one intact, two incomplete and one questionable.
Figure 6
Figure 6
Biosynthetic gene clusters (BCGs) for Lp. plantarum BRD3A HlyD-Accessory factor for PInH, LanT-Bacteriocin ABC-transporter, ATP-binding, and permease protein PInG. Plantaricin EPlantaricin F: gg motif; Lactococcin; Bacteriocin_IIc; 171.2; Plantaricin_F, Enterocin_*_chain_beta-ComC; Lactococcin; Bacteriocin_IIc; 97.2; Enterocin_X _chain beta.
Figure 7
Figure 7
Secondary metabolites prediction in the Lp. plantarum BRD3A genome by antiSMASH showing RiPP metabolites (Coagulin) highest score similarity by MIBiG database.
Figure 8
Figure 8
(A) Growth kinetics and dynamics studies of bacteriocin production at different time intervals, (B) Time kill studies of Methicillin-resistant Staphylococcus aureus ATCC 33591 showing bactericidal effect after 4 h treatment with BRDA, (C) Biofilm inhibition of BRD3A against MRSA, and (D) Field emission SEM image in (3.00X) magnification shows MRSA untreated biofilm (control) and when MRSA biofilm treated with BRD3A it showed disruption of biofilm matrix.
See this image and copyright information in PMC

References

    1. Alcock B. P., Huynh W., Chalil R., Smith K. W., Raphenya A. R., Wlodarski M. A., et al. . (2023). CARD 2023: expanded curation, support for machine learning, and resistome prediction at the Comprehensive Antibiotic Resistance Database. Nucl. Acids Res. 51, D690–D699. 10.1093/nar/gkac920 - DOI - PMC - PubMed
    1. Ali Alghamdi B., Al-Johani I., Al-Shamrani J. M., Musamed Alshamrani H., Al-Otaibi B. G., Almazmomi K., et al. . (2023). Antimicrobial resistance in methicillin-resistant staphylococcus aureus. Saudi J. Biol. Sci. 30, 103604. 10.1016/j.sjbs.2023.103604 - DOI - PMC - PubMed
    1. Andrews S. (2010). FastQC: A Quality Control Tool for High Throughput Sequence Data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc (accessed July 14, 2021).
    1. Arndt D., Grant J. R., Marcu A., Sajed T., Pon A., Liang Y., et al. . (2016). PHASTER: a better, faster version of the PHAST phage search tool. Nucl. Acids. Res. 44, W16–W21. 10.1093/nar/gkw387 - DOI - PMC - PubMed
    1. Aziz R. K., Bartels D., Best A. A., DeJongh M., Disz T., Edwards R. A., et al. . (2008). The RAST Server: rapid annotations using subsystems technology. BMC Genom. 9, 1–15. 10.1186/1471-2164-9-75 - DOI - PMC - PubMed

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