Genomic insights into the probiotic potential and genes linked to gallic acid metabolism in Pediococcus pentosaceus MBBL6 isolated from healthy cow milk.

Pediococcus pentosaceus is well known for its probiotic properties, including roles in improving health, antimicrobial production, and enhancing fermented food quality. This study aimed to comprehensively analyze the whole genome of P. pentosaceus MBBL6, isolated from healthy cow milk, to assess its...

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Main Authors: Md Morshedur Rahman, Naim Siddique, Soharth Hasnat, Md Tanvir Rahman, Mustafizur Rahman, Munirul Alam, Ziban Chandra Das, Tofazzal Islam, M Nazmul Hoque
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0316270
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author Md Morshedur Rahman
Naim Siddique
Soharth Hasnat
Md Tanvir Rahman
Mustafizur Rahman
Munirul Alam
Ziban Chandra Das
Tofazzal Islam
M Nazmul Hoque
author_facet Md Morshedur Rahman
Naim Siddique
Soharth Hasnat
Md Tanvir Rahman
Mustafizur Rahman
Munirul Alam
Ziban Chandra Das
Tofazzal Islam
M Nazmul Hoque
author_sort Md Morshedur Rahman
collection DOAJ
description Pediococcus pentosaceus is well known for its probiotic properties, including roles in improving health, antimicrobial production, and enhancing fermented food quality. This study aimed to comprehensively analyze the whole genome of P. pentosaceus MBBL6, isolated from healthy cow milk, to assess its probiotic and antimicrobial potentials. P. pentosaceus MBBL6, isolated from a healthy cow milk at BSMRAU dairy farm, Gazipur, Bangladesh, underwent comprehensive genomic analysis, including whole genome sequencing, assembly, annotation, phylogenetic comparison, and assessment of metabolic pathways and secondary metabolites. Antimicrobial efficacy was evaluated through in-vitro and in-vivo studies, alongside in-silico exploration for potential mastitis therapy. We predicted 1,906 genes and 204 SEED sub-systems involved in carbohydrate metabolism and vitamin B complex biosynthesis, with a focus on lactose metabolism in MMBL6. Notably, 43 putative carbohydrate-active enzyme genes, including lysozymes, suggest the ability of MBBL6 for carbohydrate biotransformation and antimicrobial activity. The genome also revealed primary metabolic pathways for arginine and gallic acid metabolism and secondary metabolite gene clusters, including T3PKS and RiPP-like regions. Importantly, two bacteriocin biosynthesis gene clusters namely bovicin_255_variant and penocin_A, were identified in MBBL6. The safety assessment of MBBL6 genome revealed no virulence genes and a low pathogenicity score (0.196 out of 1.0). Several genes related to survival in gastrointestinal tract and colonization were also identified. Furthermore, MBBL6 exhibited susceptibility to a wide range of antibiotics in-vitro, and effectively suppressed mastitis pathogens in an in-vivo mouse mastitis model trial. The observed bacteriocin, particularly bovicin, demonstrated the ability to disrupt the function of an essential protein, Rho factor of mastitis pathogens by blocking transcription termination process. Taken together, our in-depth genomic analysis underscores the metabolic versatility, safety profile, and antimicrobial potential of P. pentosaceus MBBL6, suggesting its promise for applications in therapeutics, bioremediation, and biopreservation.
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spelling doaj-art-ecbe4bdcd8554664b8331fc55cced5432025-01-08T05:32:28ZengPublic Library of Science (PLoS)PLoS ONE1932-62032024-01-011912e031627010.1371/journal.pone.0316270Genomic insights into the probiotic potential and genes linked to gallic acid metabolism in Pediococcus pentosaceus MBBL6 isolated from healthy cow milk.Md Morshedur RahmanNaim SiddiqueSoharth HasnatMd Tanvir RahmanMustafizur RahmanMunirul AlamZiban Chandra DasTofazzal IslamM Nazmul HoquePediococcus pentosaceus is well known for its probiotic properties, including roles in improving health, antimicrobial production, and enhancing fermented food quality. This study aimed to comprehensively analyze the whole genome of P. pentosaceus MBBL6, isolated from healthy cow milk, to assess its probiotic and antimicrobial potentials. P. pentosaceus MBBL6, isolated from a healthy cow milk at BSMRAU dairy farm, Gazipur, Bangladesh, underwent comprehensive genomic analysis, including whole genome sequencing, assembly, annotation, phylogenetic comparison, and assessment of metabolic pathways and secondary metabolites. Antimicrobial efficacy was evaluated through in-vitro and in-vivo studies, alongside in-silico exploration for potential mastitis therapy. We predicted 1,906 genes and 204 SEED sub-systems involved in carbohydrate metabolism and vitamin B complex biosynthesis, with a focus on lactose metabolism in MMBL6. Notably, 43 putative carbohydrate-active enzyme genes, including lysozymes, suggest the ability of MBBL6 for carbohydrate biotransformation and antimicrobial activity. The genome also revealed primary metabolic pathways for arginine and gallic acid metabolism and secondary metabolite gene clusters, including T3PKS and RiPP-like regions. Importantly, two bacteriocin biosynthesis gene clusters namely bovicin_255_variant and penocin_A, were identified in MBBL6. The safety assessment of MBBL6 genome revealed no virulence genes and a low pathogenicity score (0.196 out of 1.0). Several genes related to survival in gastrointestinal tract and colonization were also identified. Furthermore, MBBL6 exhibited susceptibility to a wide range of antibiotics in-vitro, and effectively suppressed mastitis pathogens in an in-vivo mouse mastitis model trial. The observed bacteriocin, particularly bovicin, demonstrated the ability to disrupt the function of an essential protein, Rho factor of mastitis pathogens by blocking transcription termination process. Taken together, our in-depth genomic analysis underscores the metabolic versatility, safety profile, and antimicrobial potential of P. pentosaceus MBBL6, suggesting its promise for applications in therapeutics, bioremediation, and biopreservation.https://doi.org/10.1371/journal.pone.0316270
spellingShingle Md Morshedur Rahman
Naim Siddique
Soharth Hasnat
Md Tanvir Rahman
Mustafizur Rahman
Munirul Alam
Ziban Chandra Das
Tofazzal Islam
M Nazmul Hoque
Genomic insights into the probiotic potential and genes linked to gallic acid metabolism in Pediococcus pentosaceus MBBL6 isolated from healthy cow milk.
PLoS ONE
title Genomic insights into the probiotic potential and genes linked to gallic acid metabolism in Pediococcus pentosaceus MBBL6 isolated from healthy cow milk.
title_full Genomic insights into the probiotic potential and genes linked to gallic acid metabolism in Pediococcus pentosaceus MBBL6 isolated from healthy cow milk.
title_fullStr Genomic insights into the probiotic potential and genes linked to gallic acid metabolism in Pediococcus pentosaceus MBBL6 isolated from healthy cow milk.
title_full_unstemmed Genomic insights into the probiotic potential and genes linked to gallic acid metabolism in Pediococcus pentosaceus MBBL6 isolated from healthy cow milk.
title_short Genomic insights into the probiotic potential and genes linked to gallic acid metabolism in Pediococcus pentosaceus MBBL6 isolated from healthy cow milk.
title_sort genomic insights into the probiotic potential and genes linked to gallic acid metabolism in pediococcus pentosaceus mbbl6 isolated from healthy cow milk
url https://doi.org/10.1371/journal.pone.0316270
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