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Article: A systematically biosynthetic investigation of lactic acid bacteria reveals diverse antagonistic bacteriocins that potentially shape the human microbiome

TitleA systematically biosynthetic investigation of lactic acid bacteria reveals diverse antagonistic bacteriocins that potentially shape the human microbiome
Authors
KeywordsBacteriocins
Biosynthetic gene clusters
Human microbiome
Lactic acid bacteria
Secondary metabolites
Vaginal microbiome
Issue Date27-Apr-2023
PublisherBioMed Central
Citation
Microbiome, 2023, v. 11, n. 1 How to Cite?
Abstract

Background

Lactic acid bacteria (LAB) produce various bioactive secondary metabolites (SMs), which endow LAB with a protective role for the host. However, the biosynthetic potentials of LAB-derived SMs remain elusive, particularly in their diversity, abundance, and distribution in the human microbiome. Thus, it is still unknown to what extent LAB-derived SMs are involved in microbiome homeostasis.

Results

Here, we systematically investigate the biosynthetic potential of LAB from 31,977 LAB genomes, identifying 130,051 secondary metabolite biosynthetic gene clusters (BGCs) of 2,849 gene cluster families (GCFs). Most of these GCFs are species-specific or even strain-specific and uncharacterized yet. Analyzing 748 human-associated metagenomes, we gain an insight into the profile of LAB BGCs, which are highly diverse and niche-specific in the human microbiome. We discover that most LAB BGCs may encode bacteriocins with pervasive antagonistic activities predicted by machine learning models, potentially playing protective roles in the human microbiome. Class II bacteriocins, one of the most abundant and diverse LAB SMs, are particularly enriched and predominant in the vaginal microbiome. We utilized metagenomic and metatranscriptomic analyses to guide our discovery of functional class II bacteriocins. Our findings suggest that these antibacterial bacteriocins have the potential to regulate microbial communities in the vagina, thereby contributing to the maintenance of microbiome homeostasis.

Conclusions

Our study systematically investigates LAB biosynthetic potential and their profiles in the human microbiome, linking them to the antagonistic contributions to microbiome homeostasis via omics analysis. These discoveries of the diverse and prevalent antagonistic SMs are expected to stimulate the mechanism study of LAB’s protective roles for the microbiome and host, highlighting the potential of LAB and their bacteriocins as therapeutic alternatives.


Persistent Identifierhttp://hdl.handle.net/10722/331309
ISSN
2023 Impact Factor: 13.8
2023 SCImago Journal Rankings: 3.802
ISI Accession Number ID

 

DC FieldValueLanguage
dc.contributor.authorZhang, DW-
dc.contributor.authorZhang, J-
dc.contributor.authorKalimuthu, S-
dc.contributor.authorLiu, J-
dc.contributor.authorSong, ZM-
dc.contributor.authorHe, BB-
dc.contributor.authorCai, PY-
dc.contributor.authorZhong, Z-
dc.contributor.authorFeng, CC-
dc.contributor.authorNeelakantan, P-
dc.contributor.authorLi, YX-
dc.date.accessioned2023-09-21T06:54:34Z-
dc.date.available2023-09-21T06:54:34Z-
dc.date.issued2023-04-27-
dc.identifier.citationMicrobiome, 2023, v. 11, n. 1-
dc.identifier.issn2049-2618-
dc.identifier.urihttp://hdl.handle.net/10722/331309-
dc.description.abstract<h3>Background</h3><p>Lactic acid bacteria (LAB) produce various bioactive secondary metabolites (SMs), which endow LAB with a protective role for the host. However, the biosynthetic potentials of LAB-derived SMs remain elusive, particularly in their diversity, abundance, and distribution in the human microbiome. Thus, it is still unknown to what extent LAB-derived SMs are involved in microbiome homeostasis.</p><h3>Results</h3><p>Here, we systematically investigate the biosynthetic potential of LAB from 31,977 LAB genomes, identifying 130,051 secondary metabolite biosynthetic gene clusters (BGCs) of 2,849 gene cluster families (GCFs). Most of these GCFs are species-specific or even strain-specific and uncharacterized yet. Analyzing 748 human-associated metagenomes, we gain an insight into the profile of LAB BGCs, which are highly diverse and niche-specific in the human microbiome. We discover that most LAB BGCs may encode bacteriocins with pervasive antagonistic activities predicted by machine learning models, potentially playing protective roles in the human microbiome. Class II bacteriocins, one of the most abundant and diverse LAB SMs, are particularly enriched and predominant in the vaginal microbiome. We utilized metagenomic and metatranscriptomic analyses to guide our discovery of functional class II bacteriocins. Our findings suggest that these antibacterial bacteriocins have the potential to regulate microbial communities in the vagina, thereby contributing to the maintenance of microbiome homeostasis.</p><h3>Conclusions</h3><p>Our study systematically investigates LAB biosynthetic potential and their profiles in the human microbiome, linking them to the antagonistic contributions to microbiome homeostasis via omics analysis. These discoveries of the diverse and prevalent antagonistic SMs are expected to stimulate the mechanism study of LAB’s protective roles for the microbiome and host, highlighting the potential of LAB and their bacteriocins as therapeutic alternatives.</p>-
dc.languageeng-
dc.publisherBioMed Central-
dc.relation.ispartofMicrobiome-
dc.rightsThis work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.-
dc.subjectBacteriocins-
dc.subjectBiosynthetic gene clusters-
dc.subjectHuman microbiome-
dc.subjectLactic acid bacteria-
dc.subjectSecondary metabolites-
dc.subjectVaginal microbiome-
dc.titleA systematically biosynthetic investigation of lactic acid bacteria reveals diverse antagonistic bacteriocins that potentially shape the human microbiome-
dc.typeArticle-
dc.description.naturepublished_or_final_version-
dc.identifier.doi10.1186/s40168-023-01540-y-
dc.identifier.scopuseid_2-s2.0-85153916195-
dc.identifier.volume11-
dc.identifier.issue1-
dc.identifier.eissn2049-2618-
dc.identifier.isiWOS:000979699200001-
dc.identifier.issnl2049-2618-

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