Metapopulation Structure of CRISPR-Cas Immunity in <italic toggle="yes">Pseudomonas aeruginosa</italic> and Its Viruses

ABSTRACT Viruses that infect the widespread opportunistic pathogen Pseudomonas aeruginosa have been shown to influence physiology and critical clinical outcomes in cystic fibrosis (CF) patients. To understand how CRISPR-Cas immune interactions may contribute to the distribution and coevolution of P....

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Autores principales:	Whitney E. England, Ted Kim, Rachel J. Whitaker
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	CRISPR Pseudomonas aeruginosa bacteriophage evolution cystic fibrosis evolution host-virus interactions Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d4d0d7b4ee5741d684c1dcd00ef51045
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spelling	oai:doaj.org-article:d4d0d7b4ee5741d684c1dcd00ef510452021-12-02T19:46:18ZMetapopulation Structure of CRISPR-Cas Immunity in <italic toggle="yes">Pseudomonas aeruginosa</italic> and Its Viruses10.1128/mSystems.00075-182379-5077https://doaj.org/article/d4d0d7b4ee5741d684c1dcd00ef510452018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00075-18https://doaj.org/toc/2379-5077ABSTRACT Viruses that infect the widespread opportunistic pathogen Pseudomonas aeruginosa have been shown to influence physiology and critical clinical outcomes in cystic fibrosis (CF) patients. To understand how CRISPR-Cas immune interactions may contribute to the distribution and coevolution of P. aeruginosa and its viruses, we reconstructed CRISPR arrays from a highly sampled longitudinal data set from CF patients attending the Copenhagen Cystic Fibrosis Clinic in Copenhagen, Denmark (R. L. Marvig, L. M. Sommer, S. Molin, and H. K. Johansen, Nat Genet 47:57–64, 2015, https://doi.org/10.1038/ng.3148). We show that new spacers are not added to or deleted from CRISPR arrays over time within a single patient but do vary among patients in this data set. We compared assembled CRISPR arrays from this data set to CRISPR arrays extracted from 726 additional publicly available P. aeruginosa sequences to show that local diversity in this population encompasses global diversity and that there is no evidence for population structure associated with location or environment sampled. We compare over 3,000 spacers from our global data set to 98 lytic and temperate viruses and proviruses and find a subset of related temperate virus clusters frequently targeted by CRISPR spacers. Highly targeted viruses are matched by different spacers in different arrays, resulting in a pattern of distributed immunity within the global population. Understanding the multiple immune contexts that P. aeruginosa viruses face can be applied to study of P. aeruginosa gene transfer, the spread of epidemic strains in cystic fibrosis patients, and viral control of P. aeruginosa infection. IMPORTANCE Pseudomonas aeruginosa is a widespread opportunistic pathogen and a major cause of morbidity and mortality in cystic fibrosis patients. Microbe-virus interactions play a critical role in shaping microbial populations, as viral infections can kill microbial populations or contribute to gene flow among microbes. Investigating how P. aeruginosa uses its CRISPR immune system to evade viral infection aids our understanding of how this organism spreads and evolves alongside its viruses in humans and the environment. Here, we identify patterns of CRISPR targeting and immunity that indicate P. aeruginosa and its viruses evolve in both a broad global population and in isolated human “islands.” These data set the stage for exploring metapopulation dynamics occurring within and between isolated “island” populations associated with CF patients, an essential step to inform future work predicting the specificity and efficacy of virus therapy and the spread of invasive viral elements and pathogenic epidemic bacterial strains.Whitney E. EnglandTed KimRachel J. WhitakerAmerican Society for MicrobiologyarticleCRISPRPseudomonas aeruginosabacteriophage evolutioncystic fibrosisevolutionhost-virus interactionsMicrobiologyQR1-502ENmSystems, Vol 3, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	CRISPR Pseudomonas aeruginosa bacteriophage evolution cystic fibrosis evolution host-virus interactions Microbiology QR1-502
spellingShingle	CRISPR Pseudomonas aeruginosa bacteriophage evolution cystic fibrosis evolution host-virus interactions Microbiology QR1-502 Whitney E. England Ted Kim Rachel J. Whitaker Metapopulation Structure of CRISPR-Cas Immunity in <italic toggle="yes">Pseudomonas aeruginosa</italic> and Its Viruses
description	ABSTRACT Viruses that infect the widespread opportunistic pathogen Pseudomonas aeruginosa have been shown to influence physiology and critical clinical outcomes in cystic fibrosis (CF) patients. To understand how CRISPR-Cas immune interactions may contribute to the distribution and coevolution of P. aeruginosa and its viruses, we reconstructed CRISPR arrays from a highly sampled longitudinal data set from CF patients attending the Copenhagen Cystic Fibrosis Clinic in Copenhagen, Denmark (R. L. Marvig, L. M. Sommer, S. Molin, and H. K. Johansen, Nat Genet 47:57–64, 2015, https://doi.org/10.1038/ng.3148). We show that new spacers are not added to or deleted from CRISPR arrays over time within a single patient but do vary among patients in this data set. We compared assembled CRISPR arrays from this data set to CRISPR arrays extracted from 726 additional publicly available P. aeruginosa sequences to show that local diversity in this population encompasses global diversity and that there is no evidence for population structure associated with location or environment sampled. We compare over 3,000 spacers from our global data set to 98 lytic and temperate viruses and proviruses and find a subset of related temperate virus clusters frequently targeted by CRISPR spacers. Highly targeted viruses are matched by different spacers in different arrays, resulting in a pattern of distributed immunity within the global population. Understanding the multiple immune contexts that P. aeruginosa viruses face can be applied to study of P. aeruginosa gene transfer, the spread of epidemic strains in cystic fibrosis patients, and viral control of P. aeruginosa infection. IMPORTANCE Pseudomonas aeruginosa is a widespread opportunistic pathogen and a major cause of morbidity and mortality in cystic fibrosis patients. Microbe-virus interactions play a critical role in shaping microbial populations, as viral infections can kill microbial populations or contribute to gene flow among microbes. Investigating how P. aeruginosa uses its CRISPR immune system to evade viral infection aids our understanding of how this organism spreads and evolves alongside its viruses in humans and the environment. Here, we identify patterns of CRISPR targeting and immunity that indicate P. aeruginosa and its viruses evolve in both a broad global population and in isolated human “islands.” These data set the stage for exploring metapopulation dynamics occurring within and between isolated “island” populations associated with CF patients, an essential step to inform future work predicting the specificity and efficacy of virus therapy and the spread of invasive viral elements and pathogenic epidemic bacterial strains.
format	article
author	Whitney E. England Ted Kim Rachel J. Whitaker
author_facet	Whitney E. England Ted Kim Rachel J. Whitaker
author_sort	Whitney E. England
title	Metapopulation Structure of CRISPR-Cas Immunity in <italic toggle="yes">Pseudomonas aeruginosa</italic> and Its Viruses
title_short	Metapopulation Structure of CRISPR-Cas Immunity in <italic toggle="yes">Pseudomonas aeruginosa</italic> and Its Viruses
title_full	Metapopulation Structure of CRISPR-Cas Immunity in <italic toggle="yes">Pseudomonas aeruginosa</italic> and Its Viruses
title_fullStr	Metapopulation Structure of CRISPR-Cas Immunity in <italic toggle="yes">Pseudomonas aeruginosa</italic> and Its Viruses
title_full_unstemmed	Metapopulation Structure of CRISPR-Cas Immunity in <italic toggle="yes">Pseudomonas aeruginosa</italic> and Its Viruses
title_sort	metapopulation structure of crispr-cas immunity in <italic toggle="yes">pseudomonas aeruginosa</italic> and its viruses
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/d4d0d7b4ee5741d684c1dcd00ef51045
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Metapopulation Structure of CRISPR-Cas Immunity in <italic toggle="yes">Pseudomonas aeruginosa</italic> and Its Viruses

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