Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations

Diseases of marine animals caused by bacteria of the genus Vibrio are on the rise worldwide. Understanding the eco-evolutionary dynamics of these infectious agents is important for predicting and managing these diseases. Yet, compared to Vibrio infecting humans, knowledge of their role as animal pat...

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Main Authors: Bruto, Maxime, Labreuche, Yannick, James, Adèle, Piel, Damien, Chenivesse, Sabine, Petton, Bruno, Le Roux, Frédérique, Polz, Martin F
Other Authors: Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Format: Article
Published: Nature Publishing Group 2018
Online Access:http://hdl.handle.net/1721.1/117414
https://orcid.org/0000-0001-9296-3733
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author Bruto, Maxime
Labreuche, Yannick
James, Adèle
Piel, Damien
Chenivesse, Sabine
Petton, Bruno
Le Roux, Frédérique
Polz, Martin F
author2 Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
author_facet Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Bruto, Maxime
Labreuche, Yannick
James, Adèle
Piel, Damien
Chenivesse, Sabine
Petton, Bruno
Le Roux, Frédérique
Polz, Martin F
author_sort Bruto, Maxime
collection MIT
description Diseases of marine animals caused by bacteria of the genus Vibrio are on the rise worldwide. Understanding the eco-evolutionary dynamics of these infectious agents is important for predicting and managing these diseases. Yet, compared to Vibrio infecting humans, knowledge of their role as animal pathogens is scarce. Here we ask how widespread is virulence among ecologically differentiated Vibrio populations, and what is the nature and frequency of virulence genes within these populations? We use a combination of population genomics and molecular genetics to assay hundreds of Vibrio strains for their virulence in the oyster Crassostrea gigas, a unique animal model that allows high-throughput infection assays. We show that within the diverse Splendidus clade, virulence represents an ancestral trait but has been lost from several populations. Two loci are necessary for virulence, the first being widely distributed across the Splendidus clade and consisting of an exported conserved protein (R5.7). The second is a MARTX toxin cluster, which only occurs within V. splendidus and is for the first time associated with virulence in marine invertebrates. Varying frequencies of both loci among populations indicate different selective pressures and alternative ecological roles, based on which we suggest strategies for epidemiological surveys.
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spelling mit-1721.1/1174142022-09-29T11:52:11Z Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations Bruto, Maxime Labreuche, Yannick James, Adèle Piel, Damien Chenivesse, Sabine Petton, Bruno Le Roux, Frédérique Polz, Martin F Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Parsons Laboratory for Environmental Science and Engineering (Massachusetts Institute of Technology) Polz, Martin F Diseases of marine animals caused by bacteria of the genus Vibrio are on the rise worldwide. Understanding the eco-evolutionary dynamics of these infectious agents is important for predicting and managing these diseases. Yet, compared to Vibrio infecting humans, knowledge of their role as animal pathogens is scarce. Here we ask how widespread is virulence among ecologically differentiated Vibrio populations, and what is the nature and frequency of virulence genes within these populations? We use a combination of population genomics and molecular genetics to assay hundreds of Vibrio strains for their virulence in the oyster Crassostrea gigas, a unique animal model that allows high-throughput infection assays. We show that within the diverse Splendidus clade, virulence represents an ancestral trait but has been lost from several populations. Two loci are necessary for virulence, the first being widely distributed across the Splendidus clade and consisting of an exported conserved protein (R5.7). The second is a MARTX toxin cluster, which only occurs within V. splendidus and is for the first time associated with virulence in marine invertebrates. Varying frequencies of both loci among populations indicate different selective pressures and alternative ecological roles, based on which we suggest strategies for epidemiological surveys. 2018-08-20T15:46:01Z 2018-08-20T15:46:01Z 2018-07 2018-06 2018-08-20T14:24:42Z Article http://purl.org/eprint/type/JournalArticle 1751-7362 1751-7370 http://hdl.handle.net/1721.1/117414 Bruto, Maxime et al. “Ancestral Gene Acquisition as the Key to Virulence Potential in Environmental Vibrio Populations.” The ISME Journal (August 2018) © 2018 The Authors https://orcid.org/0000-0001-9296-3733 http://dx.doi.org/10.1038/s41396-018-0245-3 ISME Journal Creative Commons Attribution 4.0 International License http://creativecommons.org/licenses/by/4.0/ application/pdf Nature Publishing Group Nature
spellingShingle Bruto, Maxime
Labreuche, Yannick
James, Adèle
Piel, Damien
Chenivesse, Sabine
Petton, Bruno
Le Roux, Frédérique
Polz, Martin F
Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title_full Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title_fullStr Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title_full_unstemmed Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title_short Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations
title_sort ancestral gene acquisition as the key to virulence potential in environmental vibrio populations
url http://hdl.handle.net/1721.1/117414
https://orcid.org/0000-0001-9296-3733
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