Cargando…

A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome

Vibrio cholerae-specific bacteriophages are common features of the microbial community during cholera infection in humans. Phages impose strong selective pressure that favors the expansion of phage-resistant strains over their vulnerable counterparts. The mechanisms allowing virulent V. cholerae str...

Descripción completa

Detalles Bibliográficos
Autores principales: O’Hara, Brendan J., Barth, Zachary K., McKitterick, Amelia C., Seed, Kimberley D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5481146/
https://www.ncbi.nlm.nih.gov/pubmed/28594826
http://dx.doi.org/10.1371/journal.pgen.1006838
_version_ 1783245354817290240
author O’Hara, Brendan J.
Barth, Zachary K.
McKitterick, Amelia C.
Seed, Kimberley D.
author_facet O’Hara, Brendan J.
Barth, Zachary K.
McKitterick, Amelia C.
Seed, Kimberley D.
author_sort O’Hara, Brendan J.
collection PubMed
description Vibrio cholerae-specific bacteriophages are common features of the microbial community during cholera infection in humans. Phages impose strong selective pressure that favors the expansion of phage-resistant strains over their vulnerable counterparts. The mechanisms allowing virulent V. cholerae strains to defend against the ubiquitous threat of predatory phages have not been established. Here, we show that V. cholerae PLEs (phage-inducible chromosomal island-like elements) are widespread genomic islands dedicated to phage defense. Analysis of V. cholerae isolates spanning a 60-year collection period identified five unique PLEs. Remarkably, we found that all PLEs (regardless of geographic or temporal origin) respond to infection by a myovirus called ICP1, the most prominent V. cholerae phage found in cholera patient stool samples from Bangladesh. We found that PLE activity reduces phage genome replication and accelerates cell lysis following ICP1 infection, killing infected host cells and preventing the production of progeny phage. PLEs are mobilized by ICP1 infection and can spread to neighboring cells such that protection from phage predation can be horizontally acquired. Our results reveal that PLEs are a persistent feature of the V. cholerae mobilome that are adapted to providing protection from a single predatory phage and advance our understanding of how phages influence pathogen evolution.
format Online
Article
Text
id pubmed-5481146
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-54811462017-07-06 A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome O’Hara, Brendan J. Barth, Zachary K. McKitterick, Amelia C. Seed, Kimberley D. PLoS Genet Research Article Vibrio cholerae-specific bacteriophages are common features of the microbial community during cholera infection in humans. Phages impose strong selective pressure that favors the expansion of phage-resistant strains over their vulnerable counterparts. The mechanisms allowing virulent V. cholerae strains to defend against the ubiquitous threat of predatory phages have not been established. Here, we show that V. cholerae PLEs (phage-inducible chromosomal island-like elements) are widespread genomic islands dedicated to phage defense. Analysis of V. cholerae isolates spanning a 60-year collection period identified five unique PLEs. Remarkably, we found that all PLEs (regardless of geographic or temporal origin) respond to infection by a myovirus called ICP1, the most prominent V. cholerae phage found in cholera patient stool samples from Bangladesh. We found that PLE activity reduces phage genome replication and accelerates cell lysis following ICP1 infection, killing infected host cells and preventing the production of progeny phage. PLEs are mobilized by ICP1 infection and can spread to neighboring cells such that protection from phage predation can be horizontally acquired. Our results reveal that PLEs are a persistent feature of the V. cholerae mobilome that are adapted to providing protection from a single predatory phage and advance our understanding of how phages influence pathogen evolution. Public Library of Science 2017-06-08 /pmc/articles/PMC5481146/ /pubmed/28594826 http://dx.doi.org/10.1371/journal.pgen.1006838 Text en © 2017 O’Hara 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 (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
O’Hara, Brendan J.
Barth, Zachary K.
McKitterick, Amelia C.
Seed, Kimberley D.
A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome
title A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome
title_full A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome
title_fullStr A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome
title_full_unstemmed A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome
title_short A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome
title_sort highly specific phage defense system is a conserved feature of the vibrio cholerae mobilome
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5481146/
https://www.ncbi.nlm.nih.gov/pubmed/28594826
http://dx.doi.org/10.1371/journal.pgen.1006838
work_keys_str_mv AT oharabrendanj ahighlyspecificphagedefensesystemisaconservedfeatureofthevibriocholeraemobilome
AT barthzacharyk ahighlyspecificphagedefensesystemisaconservedfeatureofthevibriocholeraemobilome
AT mckitterickameliac ahighlyspecificphagedefensesystemisaconservedfeatureofthevibriocholeraemobilome
AT seedkimberleyd ahighlyspecificphagedefensesystemisaconservedfeatureofthevibriocholeraemobilome
AT oharabrendanj highlyspecificphagedefensesystemisaconservedfeatureofthevibriocholeraemobilome
AT barthzacharyk highlyspecificphagedefensesystemisaconservedfeatureofthevibriocholeraemobilome
AT mckitterickameliac highlyspecificphagedefensesystemisaconservedfeatureofthevibriocholeraemobilome
AT seedkimberleyd highlyspecificphagedefensesystemisaconservedfeatureofthevibriocholeraemobilome