Comprehensive analysis of chromosomal mobile genetic elements in the gut microbiome reveals phylum-level niche-adaptive gene pools.

Mobile genetic elements (MGEs) drive extensive horizontal transfer in the gut microbiome. This transfer could benefit human health by conferring new metabolic capabilities to commensal microbes, or it could threaten human health by spreading antibiotic resistance genes to pathogens. Despite their bi...

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Main Authors: Xiaofang Jiang, Andrew Brantley Hall, Ramnik J Xavier, Eric J Alm
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0223680
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author Xiaofang Jiang
Andrew Brantley Hall
Ramnik J Xavier
Eric J Alm
author_facet Xiaofang Jiang
Andrew Brantley Hall
Ramnik J Xavier
Eric J Alm
author_sort Xiaofang Jiang
collection DOAJ
description Mobile genetic elements (MGEs) drive extensive horizontal transfer in the gut microbiome. This transfer could benefit human health by conferring new metabolic capabilities to commensal microbes, or it could threaten human health by spreading antibiotic resistance genes to pathogens. Despite their biological importance and medical relevance, MGEs from the gut microbiome have not been systematically characterized. Here, we present a comprehensive analysis of chromosomal MGEs in the gut microbiome using a method that enables the identification of the mobilizable unit of MGEs. We curated a database of 5,219 putative MGEs encompassing seven MGE classes called ImmeDB. We observed that many MGEs carry genes that could confer an adaptive advantage to the gut environment including gene families involved in antibiotic resistance, bile salt detoxification, mucus degradation, capsular polysaccharide biosynthesis, polysaccharide utilization, and sporulation. We find that antibiotic resistance genes are more likely to be spread by conjugation via integrative conjugative elements or integrative mobilizable elements than transduction via prophages. Horizontal transfer of MGEs is extensive within phyla but rare across phyla, supporting phylum level niche-adaptive gene pools in the gut microbiome. ImmeDB will be a valuable resource for future studies on the gut microbiome and MGE communities.
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spelling doaj.art-10a3e3013efe4f13b37bede6edac4a032022-12-21T19:58:58ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-011412e022368010.1371/journal.pone.0223680Comprehensive analysis of chromosomal mobile genetic elements in the gut microbiome reveals phylum-level niche-adaptive gene pools.Xiaofang JiangAndrew Brantley HallRamnik J XavierEric J AlmMobile genetic elements (MGEs) drive extensive horizontal transfer in the gut microbiome. This transfer could benefit human health by conferring new metabolic capabilities to commensal microbes, or it could threaten human health by spreading antibiotic resistance genes to pathogens. Despite their biological importance and medical relevance, MGEs from the gut microbiome have not been systematically characterized. Here, we present a comprehensive analysis of chromosomal MGEs in the gut microbiome using a method that enables the identification of the mobilizable unit of MGEs. We curated a database of 5,219 putative MGEs encompassing seven MGE classes called ImmeDB. We observed that many MGEs carry genes that could confer an adaptive advantage to the gut environment including gene families involved in antibiotic resistance, bile salt detoxification, mucus degradation, capsular polysaccharide biosynthesis, polysaccharide utilization, and sporulation. We find that antibiotic resistance genes are more likely to be spread by conjugation via integrative conjugative elements or integrative mobilizable elements than transduction via prophages. Horizontal transfer of MGEs is extensive within phyla but rare across phyla, supporting phylum level niche-adaptive gene pools in the gut microbiome. ImmeDB will be a valuable resource for future studies on the gut microbiome and MGE communities.https://doi.org/10.1371/journal.pone.0223680
spellingShingle Xiaofang Jiang
Andrew Brantley Hall
Ramnik J Xavier
Eric J Alm
Comprehensive analysis of chromosomal mobile genetic elements in the gut microbiome reveals phylum-level niche-adaptive gene pools.
PLoS ONE
title Comprehensive analysis of chromosomal mobile genetic elements in the gut microbiome reveals phylum-level niche-adaptive gene pools.
title_full Comprehensive analysis of chromosomal mobile genetic elements in the gut microbiome reveals phylum-level niche-adaptive gene pools.
title_fullStr Comprehensive analysis of chromosomal mobile genetic elements in the gut microbiome reveals phylum-level niche-adaptive gene pools.
title_full_unstemmed Comprehensive analysis of chromosomal mobile genetic elements in the gut microbiome reveals phylum-level niche-adaptive gene pools.
title_short Comprehensive analysis of chromosomal mobile genetic elements in the gut microbiome reveals phylum-level niche-adaptive gene pools.
title_sort comprehensive analysis of chromosomal mobile genetic elements in the gut microbiome reveals phylum level niche adaptive gene pools
url https://doi.org/10.1371/journal.pone.0223680
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