Cargando…

Quorum Sensing Determines the Choice of Antiphage Defense Strategy in Vibrio anguillarum

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Tan, Demeng, Svenningsen, Sine Lo, Middelboe, Mathias
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society of Microbiology 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4471561/
https://www.ncbi.nlm.nih.gov/pubmed/26081633
http://dx.doi.org/10.1128/mBio.00627-15
_version_ 1782376935156875264
author Tan, Demeng
Svenningsen, Sine Lo
Middelboe, Mathias
author_facet Tan, Demeng
Svenningsen, Sine Lo
Middelboe, Mathias
author_sort Tan, Demeng
collection PubMed
description 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.
format Online
Article
Text
id pubmed-4471561
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher American Society of Microbiology
record_format MEDLINE/PubMed
spelling pubmed-44715612015-06-19 Quorum Sensing Determines the Choice of Antiphage Defense Strategy in Vibrio anguillarum Tan, Demeng Svenningsen, Sine Lo Middelboe, Mathias mBio Research Article 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. American Society of Microbiology 2015-06-16 /pmc/articles/PMC4471561/ /pubmed/26081633 http://dx.doi.org/10.1128/mBio.00627-15 Text en Copyright © 2015 Tan et al. http://creativecommons.org/licenses/by-nc-sa/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license (http://creativecommons.org/licenses/by-nc-sa/3.0/) , which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Tan, Demeng
Svenningsen, Sine Lo
Middelboe, Mathias
Quorum Sensing Determines the Choice of Antiphage Defense Strategy in Vibrio anguillarum
title Quorum Sensing Determines the Choice of Antiphage Defense Strategy in Vibrio anguillarum
title_full Quorum Sensing Determines the Choice of Antiphage Defense Strategy in Vibrio anguillarum
title_fullStr Quorum Sensing Determines the Choice of Antiphage Defense Strategy in Vibrio anguillarum
title_full_unstemmed Quorum Sensing Determines the Choice of Antiphage Defense Strategy in Vibrio anguillarum
title_short Quorum Sensing Determines the Choice of Antiphage Defense Strategy in Vibrio anguillarum
title_sort quorum sensing determines the choice of antiphage defense strategy in vibrio anguillarum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4471561/
https://www.ncbi.nlm.nih.gov/pubmed/26081633
http://dx.doi.org/10.1128/mBio.00627-15
work_keys_str_mv AT tandemeng quorumsensingdeterminesthechoiceofantiphagedefensestrategyinvibrioanguillarum
AT svenningsensinelo quorumsensingdeterminesthechoiceofantiphagedefensestrategyinvibrioanguillarum
AT middelboemathias quorumsensingdeterminesthechoiceofantiphagedefensestrategyinvibrioanguillarum