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Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus

Bacteria impact humans, industry and nature, but do so under viral constraints. Problematically, knowledge of viral infection efficiencies and outcomes derives from few model systems that over-represent efficient lytic infections and under-represent virus–host natural diversity. Here we sought to un...

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Autores principales: Howard-Varona, Cristina, Roux, Simon, Dore, Hugo, Solonenko, Natalie E, Holmfeldt, Karin, Markillie, Lye M, Orr, Galya, Sullivan, Matthew B
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5335546/
https://www.ncbi.nlm.nih.gov/pubmed/27187794
http://dx.doi.org/10.1038/ismej.2016.81
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author Howard-Varona, Cristina
Roux, Simon
Dore, Hugo
Solonenko, Natalie E
Holmfeldt, Karin
Markillie, Lye M
Orr, Galya
Sullivan, Matthew B
author_facet Howard-Varona, Cristina
Roux, Simon
Dore, Hugo
Solonenko, Natalie E
Holmfeldt, Karin
Markillie, Lye M
Orr, Galya
Sullivan, Matthew B
author_sort Howard-Varona, Cristina
collection PubMed
description Bacteria impact humans, industry and nature, but do so under viral constraints. Problematically, knowledge of viral infection efficiencies and outcomes derives from few model systems that over-represent efficient lytic infections and under-represent virus–host natural diversity. Here we sought to understand infection efficiency regulation in an emerging environmental Bacteroidetes–virus model system with markedly different outcomes on two genetically and physiologically nearly identical host strains. For this, we quantified bacterial virus (phage) and host DNA, transcripts and phage particles throughout both infections. While phage transcriptomes were similar, transcriptional differences between hosts suggested host-derived regulation of infection efficiency. Specifically, the alternative host overexpressed DNA degradation genes and underexpressed translation genes, which seemingly targeted phage DNA particle production, as experiments revealed they were both significantly delayed (by >30 min) and reduced (by >50%) in the inefficient infection. This suggests phage failure to repress early alternative host expression and stress response allowed the host to respond against infection by delaying phage DNA replication and protein translation. Given that this phage type is ubiquitous and abundant in the global oceans and that variable viral infection efficiencies are central to dynamic ecosystems, these data provide a critically needed foundation for understanding and modeling viral infections in nature.
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spelling pubmed-53355462017-03-06 Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus Howard-Varona, Cristina Roux, Simon Dore, Hugo Solonenko, Natalie E Holmfeldt, Karin Markillie, Lye M Orr, Galya Sullivan, Matthew B ISME J Original Article Bacteria impact humans, industry and nature, but do so under viral constraints. Problematically, knowledge of viral infection efficiencies and outcomes derives from few model systems that over-represent efficient lytic infections and under-represent virus–host natural diversity. Here we sought to understand infection efficiency regulation in an emerging environmental Bacteroidetes–virus model system with markedly different outcomes on two genetically and physiologically nearly identical host strains. For this, we quantified bacterial virus (phage) and host DNA, transcripts and phage particles throughout both infections. While phage transcriptomes were similar, transcriptional differences between hosts suggested host-derived regulation of infection efficiency. Specifically, the alternative host overexpressed DNA degradation genes and underexpressed translation genes, which seemingly targeted phage DNA particle production, as experiments revealed they were both significantly delayed (by >30 min) and reduced (by >50%) in the inefficient infection. This suggests phage failure to repress early alternative host expression and stress response allowed the host to respond against infection by delaying phage DNA replication and protein translation. Given that this phage type is ubiquitous and abundant in the global oceans and that variable viral infection efficiencies are central to dynamic ecosystems, these data provide a critically needed foundation for understanding and modeling viral infections in nature. Nature Publishing Group 2017-01 2016-05-17 /pmc/articles/PMC5335546/ /pubmed/27187794 http://dx.doi.org/10.1038/ismej.2016.81 Text en Copyright © 2017 International Society for Microbial Ecology http://creativecommons.org/licenses/by-nc-nd/4.0/ This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/4.0/
spellingShingle Original Article
Howard-Varona, Cristina
Roux, Simon
Dore, Hugo
Solonenko, Natalie E
Holmfeldt, Karin
Markillie, Lye M
Orr, Galya
Sullivan, Matthew B
Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus
title Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus
title_full Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus
title_fullStr Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus
title_full_unstemmed Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus
title_short Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus
title_sort regulation of infection efficiency in a globally abundant marine bacteriodetes virus
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5335546/
https://www.ncbi.nlm.nih.gov/pubmed/27187794
http://dx.doi.org/10.1038/ismej.2016.81
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