Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus

Cristina Howard-Varona, Simon Roux, Hugo Dore, Natalie E. Solonenko, Karin Holmfeldt, Lye M. Markillie, Galya Orr, Matthew Sullivan

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

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.The ISME Journal advance online publication, 17 May 2016; doi:10.1038/ismej.2016.81.

Original languageEnglish (US)
JournalISME Journal
DOIs
StateAccepted/In press - May 17 2016

Fingerprint

Bacteriophages
bacteriophages
virus
Viruses
viruses
Infection
infection
Virus Diseases
DNA
alternative hosts
translation (genetics)
Protein Biosynthesis
regulation
environmental models
host strains
DNA Replication
Transcriptome
Oceans and Seas
Genes
ecosystem dynamics

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Microbiology

Cite this

Howard-Varona, C., Roux, S., Dore, H., Solonenko, N. E., Holmfeldt, K., Markillie, L. M., ... Sullivan, M. (Accepted/In press). Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus. ISME Journal. https://doi.org/10.1038/ismej.2016.81

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.

In: ISME Journal, 17.05.2016.

Research output: Contribution to journalArticle

Howard-Varona, C, Roux, S, Dore, H, Solonenko, NE, Holmfeldt, K, Markillie, LM, Orr, G & Sullivan, M 2016, 'Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus', ISME Journal. https://doi.org/10.1038/ismej.2016.81
Howard-Varona C, Roux S, Dore H, Solonenko NE, Holmfeldt K, Markillie LM et al. Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus. ISME Journal. 2016 May 17. https://doi.org/10.1038/ismej.2016.81
Howard-Varona, Cristina ; Roux, Simon ; Dore, Hugo ; Solonenko, Natalie E. ; Holmfeldt, Karin ; Markillie, Lye M. ; Orr, Galya ; Sullivan, Matthew. / Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus. In: ISME Journal. 2016.
@article{5e01360ad8ed421ea82eb3e362999a79,
title = "Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus",
abstract = "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.The ISME Journal advance online publication, 17 May 2016; doi:10.1038/ismej.2016.81.",
author = "Cristina Howard-Varona and Simon Roux and Hugo Dore and Solonenko, {Natalie E.} and Karin Holmfeldt and Markillie, {Lye M.} and Galya Orr and Matthew Sullivan",
year = "2016",
month = "5",
day = "17",
doi = "10.1038/ismej.2016.81",
language = "English (US)",
journal = "ISME Journal",
issn = "1751-7362",
publisher = "Nature Publishing Group",

}

TY - JOUR

T1 - Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus

AU - Howard-Varona, Cristina

AU - Roux, Simon

AU - Dore, Hugo

AU - Solonenko, Natalie E.

AU - Holmfeldt, Karin

AU - Markillie, Lye M.

AU - Orr, Galya

AU - Sullivan, Matthew

PY - 2016/5/17

Y1 - 2016/5/17

N2 - 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.The ISME Journal advance online publication, 17 May 2016; doi:10.1038/ismej.2016.81.

AB - 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.The ISME Journal advance online publication, 17 May 2016; doi:10.1038/ismej.2016.81.

UR - http://www.scopus.com/inward/record.url?scp=84969242986&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84969242986&partnerID=8YFLogxK

U2 - 10.1038/ismej.2016.81

DO - 10.1038/ismej.2016.81

M3 - Article

C2 - 27187794

AN - SCOPUS:84969242986

JO - ISME Journal

JF - ISME Journal

SN - 1751-7362

ER -