Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations

ABSTRACT Although plasmids and other episomes are recognized as key players in horizontal gene transfer among microbes, their diversity and dynamics among ecologically structured host populations in the wild remain poorly understood. Here, we show that natural populations of marine Vibrionaceae bact...

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Autores principales:	Hong Xue, Otto X. Cordero, Francisco M. Camas, William Trimble, Folker Meyer, Julien Guglielmini, Eduardo P. C. Rocha, Martin F. Polz
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0213fa2ab0554b7793de29ad0de85d42
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spelling	oai:doaj.org-article:0213fa2ab0554b7793de29ad0de85d422021-11-15T15:49:02ZEco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations10.1128/mBio.00552-152150-7511https://doaj.org/article/0213fa2ab0554b7793de29ad0de85d422015-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00552-15https://doaj.org/toc/2150-7511ABSTRACT Although plasmids and other episomes are recognized as key players in horizontal gene transfer among microbes, their diversity and dynamics among ecologically structured host populations in the wild remain poorly understood. Here, we show that natural populations of marine Vibrionaceae bacteria host large numbers of families of episomes, consisting of plasmids and a surprisingly high fraction of plasmid-like temperate phages. Episomes are unevenly distributed among host populations, and contrary to the notion that high-density communities in biofilms act as hot spots of gene transfer, we identified a strong bias for episomes to occur in free-living as opposed to particle-attached cells. Mapping of episomal families onto host phylogeny shows that, with the exception of all phage and a few plasmid families, most are of recent evolutionary origin and appear to have spread rapidly by horizontal transfer. Such high eco-evolutionary turnover is particularly surprising for plasmids that are, based on previously suggested categorization, putatively nontransmissible, indicating that this type of plasmid is indeed frequently transferred by currently unknown mechanisms. Finally, analysis of recent gene transfer among plasmids reveals a network of extensive exchange connecting nearly all episomes. Genes functioning in plasmid transfer and maintenance are frequently exchanged, suggesting that plasmids can be rapidly transformed from one category to another. The broad distribution of episomes among distantly related hosts and the observed promiscuous recombination patterns show how episomes can offer their hosts rapid assembly and dissemination of novel functions. IMPORTANCE Plasmids and other episomes are an integral part of bacterial biology in all environments, yet their study is heavily biased toward their role as vectors for antibiotic resistance genes. This study presents a comprehensive analysis of all episomes within several coexisting bacterial populations of Vibrionaceae from the coastal ocean and represents the largest-yet genomic survey of episomes from a single bacterial family. The host population framework allows analysis of the eco-evolutionary dynamics at unprecedented resolution, yielding several unexpected results. These include (i) discovery of novel, nonintegrative temperate phages, (ii) revision of a class of episomes, previously termed “nontransmissible,” as highly transmissible, and (iii) surprisingly high evolutionary turnover of episomes, manifest as frequent birth, spread, and loss.Hong XueOtto X. CorderoFrancisco M. CamasWilliam TrimbleFolker MeyerJulien GuglielminiEduardo P. C. RochaMartin F. PolzAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 3 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Hong Xue Otto X. Cordero Francisco M. Camas William Trimble Folker Meyer Julien Guglielmini Eduardo P. C. Rocha Martin F. Polz Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations
description	ABSTRACT Although plasmids and other episomes are recognized as key players in horizontal gene transfer among microbes, their diversity and dynamics among ecologically structured host populations in the wild remain poorly understood. Here, we show that natural populations of marine Vibrionaceae bacteria host large numbers of families of episomes, consisting of plasmids and a surprisingly high fraction of plasmid-like temperate phages. Episomes are unevenly distributed among host populations, and contrary to the notion that high-density communities in biofilms act as hot spots of gene transfer, we identified a strong bias for episomes to occur in free-living as opposed to particle-attached cells. Mapping of episomal families onto host phylogeny shows that, with the exception of all phage and a few plasmid families, most are of recent evolutionary origin and appear to have spread rapidly by horizontal transfer. Such high eco-evolutionary turnover is particularly surprising for plasmids that are, based on previously suggested categorization, putatively nontransmissible, indicating that this type of plasmid is indeed frequently transferred by currently unknown mechanisms. Finally, analysis of recent gene transfer among plasmids reveals a network of extensive exchange connecting nearly all episomes. Genes functioning in plasmid transfer and maintenance are frequently exchanged, suggesting that plasmids can be rapidly transformed from one category to another. The broad distribution of episomes among distantly related hosts and the observed promiscuous recombination patterns show how episomes can offer their hosts rapid assembly and dissemination of novel functions. IMPORTANCE Plasmids and other episomes are an integral part of bacterial biology in all environments, yet their study is heavily biased toward their role as vectors for antibiotic resistance genes. This study presents a comprehensive analysis of all episomes within several coexisting bacterial populations of Vibrionaceae from the coastal ocean and represents the largest-yet genomic survey of episomes from a single bacterial family. The host population framework allows analysis of the eco-evolutionary dynamics at unprecedented resolution, yielding several unexpected results. These include (i) discovery of novel, nonintegrative temperate phages, (ii) revision of a class of episomes, previously termed “nontransmissible,” as highly transmissible, and (iii) surprisingly high evolutionary turnover of episomes, manifest as frequent birth, spread, and loss.
format	article
author	Hong Xue Otto X. Cordero Francisco M. Camas William Trimble Folker Meyer Julien Guglielmini Eduardo P. C. Rocha Martin F. Polz
author_facet	Hong Xue Otto X. Cordero Francisco M. Camas William Trimble Folker Meyer Julien Guglielmini Eduardo P. C. Rocha Martin F. Polz
author_sort	Hong Xue
title	Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations
title_short	Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations
title_full	Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations
title_fullStr	Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations
title_full_unstemmed	Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations
title_sort	eco-evolutionary dynamics of episomes among ecologically cohesive bacterial populations
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/0213fa2ab0554b7793de29ad0de85d42
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Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations

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