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...
Published in: | The ISME Journal |
---|---|
Main Authors: | , , , , , , , |
Format: | Text |
Language: | English |
Published: |
Nature Publishing Group UK
2018
|
Subjects: | |
Online Access: | http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6246604/ http://www.ncbi.nlm.nih.gov/pubmed/30072747 https://doi.org/10.1038/s41396-018-0245-3 |
id |
ftpubmed:oai:pubmedcentral.nih.gov:6246604 |
---|---|
record_format |
openpolar |
spelling |
ftpubmed:oai:pubmedcentral.nih.gov:6246604 2023-05-15T15:58:41+02:00 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 Polz, Martin F. Le Roux, Frédérique 2018-08-02 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6246604/ http://www.ncbi.nlm.nih.gov/pubmed/30072747 https://doi.org/10.1038/s41396-018-0245-3 en eng Nature Publishing Group UK http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6246604/ http://www.ncbi.nlm.nih.gov/pubmed/30072747 http://dx.doi.org/10.1038/s41396-018-0245-3 © International Society for Microbial Ecology 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. CC-BY Article Text 2018 ftpubmed https://doi.org/10.1038/s41396-018-0245-3 2018-11-25T01:32:27Z 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. Text Crassostrea gigas PubMed Central (PMC) The ISME Journal 12 12 2954 2966 |
institution |
Open Polar |
collection |
PubMed Central (PMC) |
op_collection_id |
ftpubmed |
language |
English |
topic |
Article |
spellingShingle |
Article Bruto, Maxime Labreuche, Yannick James, Adèle Piel, Damien Chenivesse, Sabine Petton, Bruno Polz, Martin F. Le Roux, Frédérique Ancestral gene acquisition as the key to virulence potential in environmental Vibrio populations |
topic_facet |
Article |
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. |
format |
Text |
author |
Bruto, Maxime Labreuche, Yannick James, Adèle Piel, Damien Chenivesse, Sabine Petton, Bruno Polz, Martin F. Le Roux, Frédérique |
author_facet |
Bruto, Maxime Labreuche, Yannick James, Adèle Piel, Damien Chenivesse, Sabine Petton, Bruno Polz, Martin F. Le Roux, Frédérique |
author_sort |
Bruto, Maxime |
title |
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_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_sort |
ancestral gene acquisition as the key to virulence potential in environmental vibrio populations |
publisher |
Nature Publishing Group UK |
publishDate |
2018 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6246604/ http://www.ncbi.nlm.nih.gov/pubmed/30072747 https://doi.org/10.1038/s41396-018-0245-3 |
genre |
Crassostrea gigas |
genre_facet |
Crassostrea gigas |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6246604/ http://www.ncbi.nlm.nih.gov/pubmed/30072747 http://dx.doi.org/10.1038/s41396-018-0245-3 |
op_rights |
© International Society for Microbial Ecology 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. |
op_rightsnorm |
CC-BY |
op_doi |
https://doi.org/10.1038/s41396-018-0245-3 |
container_title |
The ISME Journal |
container_volume |
12 |
container_issue |
12 |
container_start_page |
2954 |
op_container_end_page |
2966 |
_version_ |
1766394447920103424 |