Model for a novel membrane envelope in a filamentous hyperthermophilic virus

Abstract
Data availability
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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.

Data availability

The following data sets were generated

1. Egelman et al.
(2017) Cryo-EM map
EMD-8780.

https://www.ebi.ac.uk/pdbe/entry/emdb/EMD-8780
1. Egelman et al.
(2017) Atomic Model
5W7G.

http://www.rcsb.org/pdb/search/structidSearch.do?structureId=5W7G

Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0003-4844-5212
Peter M Kasson

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

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-3111-8103
Frank DiMaio

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

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-7524-8938
Xiong Yu

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

Competing interests
No competing interests declared.
Soizick Lucas-Staat

Department of Microbiology, Institut Pasteur, Paris, France

Competing interests
No competing interests declared.
Mart Krupovic

Department of Microbiology, Institut Pasteur, Paris, France

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-5486-0098
Stefan Schouten

Department of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research, Texel, Netherlands

Competing interests
No competing interests declared.
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.

Copyright

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.