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The effect of a temperature‐sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen

Viruses are key actors of ecosystems and have major impacts on global biogeochemical cycles. Prophages deserve particular attention as they are ubiquitous in bacterial genomes and can enter a lytic cycle when triggered by environmental conditions. We explored how temperature affects the interactions...

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Autores principales: Bruneaux, Matthieu, Ashrafi, Roghaieh, Kronholm, Ilkka, Laanto, Elina, Örmälä‐Tiznado, Anni‐Maria, Galarza, Juan A., Zihan, Chen, Kubendran Sumathi, Mruthyunjay, Ketola, Tarmo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9826266/
https://www.ncbi.nlm.nih.gov/pubmed/35917247
http://dx.doi.org/10.1111/mec.16638
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author Bruneaux, Matthieu
Ashrafi, Roghaieh
Kronholm, Ilkka
Laanto, Elina
Örmälä‐Tiznado, Anni‐Maria
Galarza, Juan A.
Zihan, Chen
Kubendran Sumathi, Mruthyunjay
Ketola, Tarmo
author_facet Bruneaux, Matthieu
Ashrafi, Roghaieh
Kronholm, Ilkka
Laanto, Elina
Örmälä‐Tiznado, Anni‐Maria
Galarza, Juan A.
Zihan, Chen
Kubendran Sumathi, Mruthyunjay
Ketola, Tarmo
author_sort Bruneaux, Matthieu
collection PubMed
description Viruses are key actors of ecosystems and have major impacts on global biogeochemical cycles. Prophages deserve particular attention as they are ubiquitous in bacterial genomes and can enter a lytic cycle when triggered by environmental conditions. We explored how temperature affects the interactions between prophages and other biological levels using an opportunistic pathogen, the bacterium Serratia marcescens, which harbours several prophages and that had undergone an evolution experiment under several temperature regimes. We found that the release of one of the prophages was temperature‐sensitive and malleable to evolutionary changes. We further discovered that the virulence of the bacterium in an insect model also evolved and was positively correlated with phage release rates. We determined through analysis of genetic and epigenetic data that changes in the bacterial outer cell wall structure possibly explain this phenomenon. We hypothezise that the temperature‐dependent phage release rate acted as a selection pressure on S. marcescens and that it resulted in modified bacterial virulence in the insect host. Our study system illustrates how viruses can mediate the influence of abiotic environmental changes to other biological levels and thus be involved in ecosystem feedback loops.
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spelling pubmed-98262662023-01-09 The effect of a temperature‐sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen Bruneaux, Matthieu Ashrafi, Roghaieh Kronholm, Ilkka Laanto, Elina Örmälä‐Tiznado, Anni‐Maria Galarza, Juan A. Zihan, Chen Kubendran Sumathi, Mruthyunjay Ketola, Tarmo Mol Ecol ORIGINAL ARTICLES Viruses are key actors of ecosystems and have major impacts on global biogeochemical cycles. Prophages deserve particular attention as they are ubiquitous in bacterial genomes and can enter a lytic cycle when triggered by environmental conditions. We explored how temperature affects the interactions between prophages and other biological levels using an opportunistic pathogen, the bacterium Serratia marcescens, which harbours several prophages and that had undergone an evolution experiment under several temperature regimes. We found that the release of one of the prophages was temperature‐sensitive and malleable to evolutionary changes. We further discovered that the virulence of the bacterium in an insect model also evolved and was positively correlated with phage release rates. We determined through analysis of genetic and epigenetic data that changes in the bacterial outer cell wall structure possibly explain this phenomenon. We hypothezise that the temperature‐dependent phage release rate acted as a selection pressure on S. marcescens and that it resulted in modified bacterial virulence in the insect host. Our study system illustrates how viruses can mediate the influence of abiotic environmental changes to other biological levels and thus be involved in ecosystem feedback loops. John Wiley and Sons Inc. 2022-09-17 2022-10 /pmc/articles/PMC9826266/ /pubmed/35917247 http://dx.doi.org/10.1111/mec.16638 Text en © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle ORIGINAL ARTICLES
Bruneaux, Matthieu
Ashrafi, Roghaieh
Kronholm, Ilkka
Laanto, Elina
Örmälä‐Tiznado, Anni‐Maria
Galarza, Juan A.
Zihan, Chen
Kubendran Sumathi, Mruthyunjay
Ketola, Tarmo
The effect of a temperature‐sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen
title The effect of a temperature‐sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen
title_full The effect of a temperature‐sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen
title_fullStr The effect of a temperature‐sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen
title_full_unstemmed The effect of a temperature‐sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen
title_short The effect of a temperature‐sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen
title_sort effect of a temperature‐sensitive prophage on the evolution of virulence in an opportunistic bacterial pathogen
topic ORIGINAL ARTICLES
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9826266/
https://www.ncbi.nlm.nih.gov/pubmed/35917247
http://dx.doi.org/10.1111/mec.16638
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