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Title: Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus

Abstract

Microbes impact human health and disease, industrial processes and natural ecosystems, but do so under the influence of viruses. Problematically, knowledge of viral infection efficiencies and outcomes (e.g. lysis, lysogeny) derives from few model systems that over-represent efficient, lytic infections and under-represent virus-host natural diversity. Here we sought to understand how infection efficiency is regulated in an environmental Bacteroidetes virus that represents a globally abundant viral group and has drastically different infection efficiencies when infecting two nearly identical bacterial strains. To this end, we quantified bacterial virus (phage) and host DNA, transcripts and phage particles throughout the infection of both bacterial hosts. While the phage transcriptome was similar during both infections, host transcriptional differences appeared to have altered infection efficiency. Specifically, host transcriptomes suggested that the phage failed to repress early host expression in the inefficient nfection, thereby allowing the host to respond against infection by delaying phage DNA replication and protein translation. Further measurements showed that phage DNA and particle production were delayed (by >30 minutes) and reduced (by >50%) in the inefficient versus efficient infection as the host over-expressed DNA degradation genes and under-expressed translation genes, respectively. Together these results suggest that multiple levels of regulation can impactmore » infection efficiencies as failure to repress host transcription allowed the host to defend against both phage DNA and protein production. Given that this phage type is ubiquitous and abundant in the global oceans and that variably efficient viral infections are likely common in any ecosystem with varying phage-host abundances and physiological states, these data provide a critically needed foundation for understanding and modeling viral infection efficiency in nature.« less

Authors:
 [1];  [2];  [3];  [2];  [4];  [5];  [5];  [6]
  1. Univ. of Arizona, Tucson, AZ (United States). Dept. of Molecular and Cellular Biology
  2. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology
  3. Ecole normale superieure de Lyon (ENS), Lyon (France)
  4. Linnaeus Univ., Kalmar (Sweden). School of Natural Sciences
  5. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
  6. Univ. of Arizona, Tucson, AZ (United States). Dept. of Molecular and Cellular Biology; Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Institutes of Health (NIH); Gordon and Betty Moore Foundation
OSTI Identifier:
1353319
Report Number(s):
PNNL-SA-115144
Journal ID: ISSN 1751-7362; 47930; KP1704020
Grant/Contract Number:  
AC05-76RL01830; 2631; 3790
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; Infection; Bacteriodetes; virus; DNA; Environmental Molecular Sciences Laboratory

Citation Formats

Howard-Varona, Cristina, Roux, Simon, Dore, Hugo, Solonenko, Natalie E., Holmfeldt, Karin, Markillie, Lye M., Orr, Galya, and Sullivan, Matthew B. Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus. United States: N. p., 2016. Web. doi:10.1038/ismej.2016.81.
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. United States. doi:10.1038/ismej.2016.81.
Howard-Varona, Cristina, Roux, Simon, Dore, Hugo, Solonenko, Natalie E., Holmfeldt, Karin, Markillie, Lye M., Orr, Galya, and Sullivan, Matthew B. Tue . "Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus". United States. doi:10.1038/ismej.2016.81. https://www.osti.gov/servlets/purl/1353319.
@article{osti_1353319,
title = {Regulation of infection efficiency in a globally abundant marine Bacteriodetes virus},
author = {Howard-Varona, Cristina and Roux, Simon and Dore, Hugo and Solonenko, Natalie E. and Holmfeldt, Karin and Markillie, Lye M. and Orr, Galya and Sullivan, Matthew B.},
abstractNote = {Microbes impact human health and disease, industrial processes and natural ecosystems, but do so under the influence of viruses. Problematically, knowledge of viral infection efficiencies and outcomes (e.g. lysis, lysogeny) derives from few model systems that over-represent efficient, lytic infections and under-represent virus-host natural diversity. Here we sought to understand how infection efficiency is regulated in an environmental Bacteroidetes virus that represents a globally abundant viral group and has drastically different infection efficiencies when infecting two nearly identical bacterial strains. To this end, we quantified bacterial virus (phage) and host DNA, transcripts and phage particles throughout the infection of both bacterial hosts. While the phage transcriptome was similar during both infections, host transcriptional differences appeared to have altered infection efficiency. Specifically, host transcriptomes suggested that the phage failed to repress early host expression in the inefficient nfection, thereby allowing the host to respond against infection by delaying phage DNA replication and protein translation. Further measurements showed that phage DNA and particle production were delayed (by >30 minutes) and reduced (by >50%) in the inefficient versus efficient infection as the host over-expressed DNA degradation genes and under-expressed translation genes, respectively. Together these results suggest that multiple levels of regulation can impact infection efficiencies as failure to repress host transcription allowed the host to defend against both phage DNA and protein production. Given that this phage type is ubiquitous and abundant in the global oceans and that variably efficient viral infections are likely common in any ecosystem with varying phage-host abundances and physiological states, these data provide a critically needed foundation for understanding and modeling viral infection efficiency in nature.},
doi = {10.1038/ismej.2016.81},
journal = {The ISME Journal},
number = 1,
volume = 11,
place = {United States},
year = {2016},
month = {5}
}

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    Works referencing / citing this record:

    Multiple mechanisms drive phage infection efficiency in nearly identical hosts
    journal, March 2018

    • Howard-Varona, Cristina; Hargreaves, Katherine R.; Solonenko, Natalie E.
    • The ISME Journal, Vol. 12, Issue 6
    • DOI: 10.1038/s41396-018-0099-8

    Multiple mechanisms drive phage infection efficiency in nearly identical hosts
    journal, March 2018

    • Howard-Varona, Cristina; Hargreaves, Katherine R.; Solonenko, Natalie E.
    • The ISME Journal, Vol. 12, Issue 6
    • DOI: 10.1038/s41396-018-0099-8