CRISPR Immunity Drives Rapid Phage Genome Evolution in <named-content content-type="genus-species">Streptococcus thermophilus</named-content>

ABSTRACT Many bacteria rely on CRISPR-Cas systems to provide adaptive immunity against phages, predation by which can shape the ecology and functioning of microbial communities. To characterize the impact of CRISPR immunization on phage genome evolution, we performed long-term bacterium-phage (Strep...

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Autores principales:	David Paez-Espino, Itai Sharon, Wesley Morovic, Buffy Stahl, Brian C. Thomas, Rodolphe Barrangou, Jillian F. Banfield
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/34119cd207cc4a53a00028261d4e0b44
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spelling	oai:doaj.org-article:34119cd207cc4a53a00028261d4e0b442021-11-15T15:41:33ZCRISPR Immunity Drives Rapid Phage Genome Evolution in <named-content content-type="genus-species">Streptococcus thermophilus</named-content>10.1128/mBio.00262-152150-7511https://doaj.org/article/34119cd207cc4a53a00028261d4e0b442015-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00262-15https://doaj.org/toc/2150-7511ABSTRACT Many bacteria rely on CRISPR-Cas systems to provide adaptive immunity against phages, predation by which can shape the ecology and functioning of microbial communities. To characterize the impact of CRISPR immunization on phage genome evolution, we performed long-term bacterium-phage (Streptococcus thermophilus-phage 2972) coevolution experiments. We found that in this species, CRISPR immunity drives fixation of single nucleotide polymorphisms that accumulate exclusively in phage genome regions targeted by CRISPR. Mutation rates in phage genomes highly exceed those of the host. The presence of multiple phages increased phage persistence by enabling recombination-based formation of chimeric phage genomes in which sequences heavily targeted by CRISPR were replaced. Collectively, our results establish CRISPR-Cas adaptive immunity as a key driver of phage genome evolution under the conditions studied and highlight the importance of multiple coexisting phages for persistence in natural systems. IMPORTANCE Phages remain an enigmatic part of the biosphere. As predators, they challenge the survival of host bacteria and archaea and set off an “arms race” involving host immunization countered by phage mutation. The CRISPR-Cas system is adaptive: by capturing fragments of a phage genome upon exposure, the host is positioned to counteract future infections. To investigate this process, we initiated massive deep-sequencing experiments with a host and infective phage and tracked the coevolution of both populations over hundreds of days. In the present study, we found that CRISPR immunity drives the accumulation of phage genome rearrangements (which enable longer phage survival) and escape mutations, establishing CRISPR as one of the fundamental drivers of phage evolution.David Paez-EspinoItai SharonWesley MorovicBuffy StahlBrian C. ThomasRodolphe BarrangouJillian F. BanfieldAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 2 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 David Paez-Espino Itai Sharon Wesley Morovic Buffy Stahl Brian C. Thomas Rodolphe Barrangou Jillian F. Banfield CRISPR Immunity Drives Rapid Phage Genome Evolution in <named-content content-type="genus-species">Streptococcus thermophilus</named-content>
description	ABSTRACT Many bacteria rely on CRISPR-Cas systems to provide adaptive immunity against phages, predation by which can shape the ecology and functioning of microbial communities. To characterize the impact of CRISPR immunization on phage genome evolution, we performed long-term bacterium-phage (Streptococcus thermophilus-phage 2972) coevolution experiments. We found that in this species, CRISPR immunity drives fixation of single nucleotide polymorphisms that accumulate exclusively in phage genome regions targeted by CRISPR. Mutation rates in phage genomes highly exceed those of the host. The presence of multiple phages increased phage persistence by enabling recombination-based formation of chimeric phage genomes in which sequences heavily targeted by CRISPR were replaced. Collectively, our results establish CRISPR-Cas adaptive immunity as a key driver of phage genome evolution under the conditions studied and highlight the importance of multiple coexisting phages for persistence in natural systems. IMPORTANCE Phages remain an enigmatic part of the biosphere. As predators, they challenge the survival of host bacteria and archaea and set off an “arms race” involving host immunization countered by phage mutation. The CRISPR-Cas system is adaptive: by capturing fragments of a phage genome upon exposure, the host is positioned to counteract future infections. To investigate this process, we initiated massive deep-sequencing experiments with a host and infective phage and tracked the coevolution of both populations over hundreds of days. In the present study, we found that CRISPR immunity drives the accumulation of phage genome rearrangements (which enable longer phage survival) and escape mutations, establishing CRISPR as one of the fundamental drivers of phage evolution.
format	article
author	David Paez-Espino Itai Sharon Wesley Morovic Buffy Stahl Brian C. Thomas Rodolphe Barrangou Jillian F. Banfield
author_facet	David Paez-Espino Itai Sharon Wesley Morovic Buffy Stahl Brian C. Thomas Rodolphe Barrangou Jillian F. Banfield
author_sort	David Paez-Espino
title	CRISPR Immunity Drives Rapid Phage Genome Evolution in <named-content content-type="genus-species">Streptococcus thermophilus</named-content>
title_short	CRISPR Immunity Drives Rapid Phage Genome Evolution in <named-content content-type="genus-species">Streptococcus thermophilus</named-content>
title_full	CRISPR Immunity Drives Rapid Phage Genome Evolution in <named-content content-type="genus-species">Streptococcus thermophilus</named-content>
title_fullStr	CRISPR Immunity Drives Rapid Phage Genome Evolution in <named-content content-type="genus-species">Streptococcus thermophilus</named-content>
title_full_unstemmed	CRISPR Immunity Drives Rapid Phage Genome Evolution in <named-content content-type="genus-species">Streptococcus thermophilus</named-content>
title_sort	crispr immunity drives rapid phage genome evolution in <named-content content-type="genus-species">streptococcus thermophilus</named-content>
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/34119cd207cc4a53a00028261d4e0b44
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CRISPR Immunity Drives Rapid Phage Genome Evolution in <named-content content-type="genus-species">Streptococcus thermophilus</named-content>

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