Model for a novel membrane envelope in a filamentous hyperthermophilic virus

  1. Edward H Egelman  Is a corresponding author
  2. Peter M Kasson
  3. Frank DiMaio
  4. Xiong Yu
  5. Soizick Lucas-Staat
  6. Mart Krupovic
  7. Stefan Schouten
  8. David Prangishvili  Is a corresponding author
  1. University of Virginia, United States
  2. University of Washington, United States
  3. Institut Pasteur, France
  4. NIOZ Royal Netherlands Institute for Sea Research, Netherlands

Abstract

Biological membranes create compartments, and are usually formed by lipid bilayers. However, in hyperthermophilic archaea that live optimally at temperatures above 80°C the membranes are monolayers which resemble fused bilayers. Many double-stranded DNA viruses which parasitize such hosts, including the filamentous virus AFV1 of Acidianus hospitalis, are enveloped with a lipid-containing membrane. Using cryo-EM, we show that the membrane in AFV1 is a ~2 nm-thick monolayer, approximately half the expected membrane thickness, formed by host membrane-derived lipids which adopt a U-shaped 'horseshoe' conformation. We hypothesize that this unusual viral envelope structure results from the extreme curvature of the viral capsid, as 'horseshoe' lipid conformations favor such curvature and host membrane lipids that permit horseshoe conformations are selectively recruited into the viral envelope. The unusual envelope found in AFV1 also has many implications for biotechnology, since this membrane can survive the most aggressive conditions involving extremes of temperature and pH.

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Author details

  1. Edward H Egelman

    Department of Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, United States
    For correspondence
    egelman@virginia.edu
    Competing interests
    Edward H Egelman, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4844-5212
  2. Peter M Kasson

    Department of Molecular Physiology and Biological Physics, University of Virginia, Charlottesville, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3111-8103
  3. Frank DiMaio

    Department of Biochemistry, University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7524-8938
  4. Xiong Yu

    Department of Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, United States
    Competing interests
    No competing interests declared.
  5. Soizick Lucas-Staat

    Department of Microbiology, Institut Pasteur, Paris, France
    Competing interests
    No competing interests declared.
  6. Mart Krupovic

    Department of Microbiology, Institut Pasteur, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5486-0098
  7. Stefan Schouten

    Department of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research, Texel, Netherlands
    Competing interests
    No competing interests declared.
  8. David Prangishvili

    Department of Microbiology, Institut Pasteur, Paris, France
    For correspondence
    david.prangishvili@pasteur.fr
    Competing interests
    No competing interests declared.

Funding

National Institutes of Health (GM035269)

  • Edward H Egelman

Agence Nationale de la Recherche (ANR-13-BSV3-0017-01)

  • David Prangishvili

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Sriram Subramaniam, National Cancer Institute, United States

Publication history

  1. Received: February 22, 2017
  2. Accepted: June 14, 2017
  3. Accepted Manuscript published: June 22, 2017 (version 1)
  4. Version of Record published: July 19, 2017 (version 2)

Copyright

© 2017, Egelman et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Edward H Egelman
  2. Peter M Kasson
  3. Frank DiMaio
  4. Xiong Yu
  5. Soizick Lucas-Staat
  6. Mart Krupovic
  7. Stefan Schouten
  8. David Prangishvili
(2017)
Model for a novel membrane envelope in a filamentous hyperthermophilic virus
eLife 6:e26268.
https://doi.org/10.7554/eLife.26268

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