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Title: 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 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 bemore » 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.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [5];  [5];  [1]
  1. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States), Parsons Laboratory for Environmental Science and Engineering
  2. Department of Environmental Systems Science, ETH Zürich, Zürich, Switzerland
  3. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States), Department of Biological Engineering
  4. Argonne National Lab. (ANL), Argonne, IL (United States), Mathematics and Computer Science Division
  5. Microbial Evolutionary Genomics, Institut Pasteur, Paris, France; CNRS, UMR3525, Paris, France
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE; National Science Foundation (NSF)
OSTI Identifier:
1214641
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Volume: 6; Journal Issue: 3; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Xue, Hong, Cordero, Otto X., Camas, Francisco M., Trimble, William, Meyer, Folker, Guglielmini, Julien, Rocha, Eduardo P. C., and Polz, Martin F. Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations. United States: N. p., 2015. Web. doi:10.1128/mBio.00552-15.
Xue, Hong, Cordero, Otto X., Camas, Francisco M., Trimble, William, Meyer, Folker, Guglielmini, Julien, Rocha, Eduardo P. C., & Polz, Martin F. Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations. United States. doi:10.1128/mBio.00552-15.
Xue, Hong, Cordero, Otto X., Camas, Francisco M., Trimble, William, Meyer, Folker, Guglielmini, Julien, Rocha, Eduardo P. C., and Polz, Martin F. Tue . "Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations". United States. doi:10.1128/mBio.00552-15. https://www.osti.gov/servlets/purl/1214641.
@article{osti_1214641,
title = {Eco-Evolutionary Dynamics of Episomes among Ecologically Cohesive Bacterial Populations},
author = {Xue, Hong and Cordero, Otto X. and Camas, Francisco M. and Trimble, William and Meyer, Folker and Guglielmini, Julien and Rocha, Eduardo P. C. and Polz, Martin F.},
abstractNote = {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.},
doi = {10.1128/mBio.00552-15},
journal = {mBio (Online)},
issn = {2150-7511},
number = 3,
volume = 6,
place = {United States},
year = {2015},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
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Cited by: 9 works
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