Quorum Sensing Determines the Choice of Antiphage Defense Strategy in <named-content content-type="genus-species">Vibrio anguillarum</named-content>

ABSTRACT Selection for phage resistance is a key driver of bacterial diversity and evolution, and phage-host interactions may therefore have strong influence on the genetic and functional dynamics of bacterial communities. In this study, we found that an important, but so far largely overlooked, det...

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Autores principales:	Demeng Tan, Sine Lo Svenningsen, Mathias Middelboe
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5b11474adef24997a26976585d64d76d
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spelling	oai:doaj.org-article:5b11474adef24997a26976585d64d76d2021-11-15T15:49:02ZQuorum Sensing Determines the Choice of Antiphage Defense Strategy in <named-content content-type="genus-species">Vibrio anguillarum</named-content>10.1128/mBio.00627-152150-7511https://doaj.org/article/5b11474adef24997a26976585d64d76d2015-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00627-15https://doaj.org/toc/2150-7511ABSTRACT Selection for phage resistance is a key driver of bacterial diversity and evolution, and phage-host interactions may therefore have strong influence on the genetic and functional dynamics of bacterial communities. In this study, we found that an important, but so far largely overlooked, determinant of the outcome of phage-bacterial encounters in the fish pathogen Vibrio anguillarum is bacterial cell-cell communication, known as quorum sensing. Specifically, V. anguillarum PF430-3 cells locked in the low-cell-density state (ΔvanT mutant) express high levels of the phage receptor OmpK, resulting in a high susceptibility to phage KVP40, but achieve protection from infection by enhanced biofilm formation. By contrast, cells locked in the high-cell-density state (ΔvanΟ mutant) are almost completely unsusceptible due to quorum-sensing-mediated downregulation of OmpK expression. The phenotypes of the two quorum-sensing mutant strains are accurately reflected in the behavior of wild-type V. anguillarum, which (i) displays increased OmpK expression in aggregated cells compared to free-living variants in the same culture, (ii) displays a clear inverse correlation between ompK mRNA levels and the concentration of N-acylhomoserine lactone quorum-sensing signals in the culture medium, and (iii) survives mainly by one of these two defense mechanisms, rather than by genetic mutation to phage resistance. Taken together, our results demonstrate that V. anguillarum employs quorum-sensing information to choose between two complementary antiphage defense strategies. Further, the prevalence of nonmutational defense mechanisms in strain PF430-3 suggests highly flexible adaptations to KVP40 phage infection pressure, possibly allowing the long-term coexistence of phage and host. IMPORTANCE Comprehensive knowledge on bacterial antiphage strategies and their regulation is essential for understanding the role of phages as drivers of bacterial evolution and diversity. In an applied context, development of successful phage-based control of bacterial pathogens also requires detailed understanding of the mechanisms of phage protection in pathogenic bacteria. Here, we demonstrate for the first time the presence of quorum-sensing-regulated phage defense mechanisms in the fish pathogen Vibrio anguillarum and provide evidence that quorum-sensing regulation allows V. anguillarum to alternate between different phage protection mechanisms depending on population cell density. Further, our results demonstrate the prevalence of nonmutational defense mechanisms in the investigated V. anguillarum strain, which allow flexible adaptations to a dynamic phage infection pressure.Demeng TanSine Lo SvenningsenMathias MiddelboeAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 3 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Demeng Tan Sine Lo Svenningsen Mathias Middelboe Quorum Sensing Determines the Choice of Antiphage Defense Strategy in <named-content content-type="genus-species">Vibrio anguillarum</named-content>
description	ABSTRACT Selection for phage resistance is a key driver of bacterial diversity and evolution, and phage-host interactions may therefore have strong influence on the genetic and functional dynamics of bacterial communities. In this study, we found that an important, but so far largely overlooked, determinant of the outcome of phage-bacterial encounters in the fish pathogen Vibrio anguillarum is bacterial cell-cell communication, known as quorum sensing. Specifically, V. anguillarum PF430-3 cells locked in the low-cell-density state (ΔvanT mutant) express high levels of the phage receptor OmpK, resulting in a high susceptibility to phage KVP40, but achieve protection from infection by enhanced biofilm formation. By contrast, cells locked in the high-cell-density state (ΔvanΟ mutant) are almost completely unsusceptible due to quorum-sensing-mediated downregulation of OmpK expression. The phenotypes of the two quorum-sensing mutant strains are accurately reflected in the behavior of wild-type V. anguillarum, which (i) displays increased OmpK expression in aggregated cells compared to free-living variants in the same culture, (ii) displays a clear inverse correlation between ompK mRNA levels and the concentration of N-acylhomoserine lactone quorum-sensing signals in the culture medium, and (iii) survives mainly by one of these two defense mechanisms, rather than by genetic mutation to phage resistance. Taken together, our results demonstrate that V. anguillarum employs quorum-sensing information to choose between two complementary antiphage defense strategies. Further, the prevalence of nonmutational defense mechanisms in strain PF430-3 suggests highly flexible adaptations to KVP40 phage infection pressure, possibly allowing the long-term coexistence of phage and host. IMPORTANCE Comprehensive knowledge on bacterial antiphage strategies and their regulation is essential for understanding the role of phages as drivers of bacterial evolution and diversity. In an applied context, development of successful phage-based control of bacterial pathogens also requires detailed understanding of the mechanisms of phage protection in pathogenic bacteria. Here, we demonstrate for the first time the presence of quorum-sensing-regulated phage defense mechanisms in the fish pathogen Vibrio anguillarum and provide evidence that quorum-sensing regulation allows V. anguillarum to alternate between different phage protection mechanisms depending on population cell density. Further, our results demonstrate the prevalence of nonmutational defense mechanisms in the investigated V. anguillarum strain, which allow flexible adaptations to a dynamic phage infection pressure.
format	article
author	Demeng Tan Sine Lo Svenningsen Mathias Middelboe
author_facet	Demeng Tan Sine Lo Svenningsen Mathias Middelboe
author_sort	Demeng Tan
title	Quorum Sensing Determines the Choice of Antiphage Defense Strategy in <named-content content-type="genus-species">Vibrio anguillarum</named-content>
title_short	Quorum Sensing Determines the Choice of Antiphage Defense Strategy in <named-content content-type="genus-species">Vibrio anguillarum</named-content>
title_full	Quorum Sensing Determines the Choice of Antiphage Defense Strategy in <named-content content-type="genus-species">Vibrio anguillarum</named-content>
title_fullStr	Quorum Sensing Determines the Choice of Antiphage Defense Strategy in <named-content content-type="genus-species">Vibrio anguillarum</named-content>
title_full_unstemmed	Quorum Sensing Determines the Choice of Antiphage Defense Strategy in <named-content content-type="genus-species">Vibrio anguillarum</named-content>
title_sort	quorum sensing determines the choice of antiphage defense strategy in <named-content content-type="genus-species">vibrio anguillarum</named-content>
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/5b11474adef24997a26976585d64d76d
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Quorum Sensing Determines the Choice of Antiphage Defense Strategy in <named-content content-type="genus-species">Vibrio anguillarum</named-content>

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