Model for a novel membrane envelope in a filamentous hyperthermophilic virus

Author:

Kasson Peter12ORCID,DiMaio Frank3ORCID,Yu Xiong4,Lucas-Staat Soizick5,Krupovic Mart5ORCID,Schouten Stefan67,Prangishvili David5,Egelman Edward H4ORCID

Affiliation:

1. Department of Molecular Physiology and Biological Physics, University of Virginia, Charlottesville, United States

2. Department of Biomedical Engineering, University of Virginia, Charlottesville, United States

3. Department of Biochemistry, University of Washington, Seattle, United States

4. Department of Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, United States

5. Department of Microbiology, Institut Pasteur, Paris, France

6. NIOZ Royal Netherlands Institute for Sea Research, Texel, Netherlands

7. Department of Marine Microbiology and Biogeochemistry, Utrecht University, Texel, 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.

Funder

National Institutes of Health

Agence Nationale de la Recherche

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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