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Enterococcus faecalis Prophage Dynamics and Contributions to Pathogenic Traits

Polylysogeny is frequently considered to be the result of an adaptive evolutionary process in which prophages confer fitness and/or virulence factors, thus making them important for evolution of both bacterial populations and infectious diseases. The Enterococcus faecalis V583 isolate belongs to the...

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Autores principales: Matos, Renata C., Lapaque, Nicolas, Rigottier-Gois, Lionel, Debarbieux, Laurent, Meylheuc, Thierry, Gonzalez-Zorn, Bruno, Repoila, Francis, Lopes, Maria de Fatima, Serror, Pascale
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3675006/
https://www.ncbi.nlm.nih.gov/pubmed/23754962
http://dx.doi.org/10.1371/journal.pgen.1003539
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author Matos, Renata C.
Lapaque, Nicolas
Rigottier-Gois, Lionel
Debarbieux, Laurent
Meylheuc, Thierry
Gonzalez-Zorn, Bruno
Repoila, Francis
Lopes, Maria de Fatima
Serror, Pascale
author_facet Matos, Renata C.
Lapaque, Nicolas
Rigottier-Gois, Lionel
Debarbieux, Laurent
Meylheuc, Thierry
Gonzalez-Zorn, Bruno
Repoila, Francis
Lopes, Maria de Fatima
Serror, Pascale
author_sort Matos, Renata C.
collection PubMed
description Polylysogeny is frequently considered to be the result of an adaptive evolutionary process in which prophages confer fitness and/or virulence factors, thus making them important for evolution of both bacterial populations and infectious diseases. The Enterococcus faecalis V583 isolate belongs to the high-risk clonal complex 2 that is particularly well adapted to the hospital environment. Its genome carries 7 prophage-like elements (V583-pp1 to -pp7), one of which is ubiquitous in the species. In this study, we investigated the activity of the V583 prophages and their contribution to E. faecalis biological traits. We systematically analyzed the ability of each prophage to excise from the bacterial chromosome, to replicate and to package its DNA. We also created a set of E. faecalis isogenic strains that lack from one to all six non-ubiquitous prophages by mimicking natural excision. Our work reveals that prophages of E. faecalis V583 excise from the bacterial chromosome in the presence of a fluoroquinolone, and are able to produce active phage progeny. Intricate interactions between V583 prophages were also unveiled: i) pp7, coined EfCIV583 for E. faecalis chromosomal island of V583, hijacks capsids from helper phage 1, leading to the formation of distinct virions, and ii) pp1, pp3 and pp5 inhibit excision of pp4 and pp6. The hijacking exerted by EfCIV583 on helper phage 1 capsids is the first example of molecular piracy in Gram positive bacteria other than staphylococci. Furthermore, prophages encoding platelet-binding-like proteins were found to be involved in adhesion to human platelets, considered as a first step towards the development of infective endocarditis. Our findings reveal not only a role of E. faecalis V583 prophages in pathogenicity, but also provide an explanation for the correlation between antibiotic usage and E. faecalis success as a nosocomial pathogen, as fluoriquinolone may provoke release of prophages and promote gene dissemination among isolates.
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spelling pubmed-36750062013-06-10 Enterococcus faecalis Prophage Dynamics and Contributions to Pathogenic Traits Matos, Renata C. Lapaque, Nicolas Rigottier-Gois, Lionel Debarbieux, Laurent Meylheuc, Thierry Gonzalez-Zorn, Bruno Repoila, Francis Lopes, Maria de Fatima Serror, Pascale PLoS Genet Research Article Polylysogeny is frequently considered to be the result of an adaptive evolutionary process in which prophages confer fitness and/or virulence factors, thus making them important for evolution of both bacterial populations and infectious diseases. The Enterococcus faecalis V583 isolate belongs to the high-risk clonal complex 2 that is particularly well adapted to the hospital environment. Its genome carries 7 prophage-like elements (V583-pp1 to -pp7), one of which is ubiquitous in the species. In this study, we investigated the activity of the V583 prophages and their contribution to E. faecalis biological traits. We systematically analyzed the ability of each prophage to excise from the bacterial chromosome, to replicate and to package its DNA. We also created a set of E. faecalis isogenic strains that lack from one to all six non-ubiquitous prophages by mimicking natural excision. Our work reveals that prophages of E. faecalis V583 excise from the bacterial chromosome in the presence of a fluoroquinolone, and are able to produce active phage progeny. Intricate interactions between V583 prophages were also unveiled: i) pp7, coined EfCIV583 for E. faecalis chromosomal island of V583, hijacks capsids from helper phage 1, leading to the formation of distinct virions, and ii) pp1, pp3 and pp5 inhibit excision of pp4 and pp6. The hijacking exerted by EfCIV583 on helper phage 1 capsids is the first example of molecular piracy in Gram positive bacteria other than staphylococci. Furthermore, prophages encoding platelet-binding-like proteins were found to be involved in adhesion to human platelets, considered as a first step towards the development of infective endocarditis. Our findings reveal not only a role of E. faecalis V583 prophages in pathogenicity, but also provide an explanation for the correlation between antibiotic usage and E. faecalis success as a nosocomial pathogen, as fluoriquinolone may provoke release of prophages and promote gene dissemination among isolates. Public Library of Science 2013-06-06 /pmc/articles/PMC3675006/ /pubmed/23754962 http://dx.doi.org/10.1371/journal.pgen.1003539 Text en © 2013 Matos et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Matos, Renata C.
Lapaque, Nicolas
Rigottier-Gois, Lionel
Debarbieux, Laurent
Meylheuc, Thierry
Gonzalez-Zorn, Bruno
Repoila, Francis
Lopes, Maria de Fatima
Serror, Pascale
Enterococcus faecalis Prophage Dynamics and Contributions to Pathogenic Traits
title Enterococcus faecalis Prophage Dynamics and Contributions to Pathogenic Traits
title_full Enterococcus faecalis Prophage Dynamics and Contributions to Pathogenic Traits
title_fullStr Enterococcus faecalis Prophage Dynamics and Contributions to Pathogenic Traits
title_full_unstemmed Enterococcus faecalis Prophage Dynamics and Contributions to Pathogenic Traits
title_short Enterococcus faecalis Prophage Dynamics and Contributions to Pathogenic Traits
title_sort enterococcus faecalis prophage dynamics and contributions to pathogenic traits
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3675006/
https://www.ncbi.nlm.nih.gov/pubmed/23754962
http://dx.doi.org/10.1371/journal.pgen.1003539
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