A virus of hyperthermophilic archaea with a unique architecture among DNA viruses

Edited by James L. Van Etten, University of Nebraska-Lincoln, Lincoln, NE, and approved January 19, 2016 (received for review September 23, 2015)
February 16, 2016
113 (9) 2478-2483

Significance

We describe a filamentous virus, Pyrobaculum filamentous virus 1 (PFV1), with a linear double-stranded DNA genome. PFV1 infects hyperthermophilic archaea of the genus Pyrobaculum and displays a virion organization that is unique among filamentous DNA viruses. With its linear genome enclosed in a tripartite shell consisting of two protein layers and an external envelope, PFV1 virion organization bears a superficial resemblance to that of filoviruses, such as Ebola and Marburg viruses, which have negative-sense RNA genomes. This observation suggests that overall similar designs in the viral world have been achieved on multiple independent occasions.

Abstract

Viruses package their genetic material in diverse ways. Most known strategies include encapsulation of nucleic acids into spherical or filamentous virions with icosahedral or helical symmetry, respectively. Filamentous viruses with dsDNA genomes are currently associated exclusively with Archaea. Here, we describe a filamentous hyperthermophilic archaeal virus, Pyrobaculum filamentous virus 1 (PFV1), with a type of virion organization not previously observed in DNA viruses. The PFV1 virion, 400 ± 20 × 32 ± 3 nm, contains an envelope and an inner core consisting of two structural units: a rod-shaped helical nucleocapsid formed of two 14-kDa major virion proteins and a nucleocapsid-encompassing protein sheath composed of a single major virion protein of 18 kDa. The virion organization of PFV1 is superficially similar to that of negative-sense RNA viruses of the family Filoviridae, including Ebola virus and Marburg virus. The linear dsDNA of PFV1 carries 17,714 bp, including 60-bp-long terminal inverted repeats, and contains 39 predicted ORFs, most of which do not show similarities to sequences in public databases. PFV1 is a lytic virus that completely disrupts the host cell membrane at the end of the infection cycle.

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Data Availability

Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession no. KU307456).

Acknowledgments

We thank Mery Pina for help in collecting environmental samples; Soizick Lucas-Staat and Jérémie Chaligné for assistance in experiments; Patrick Forterre for helpful discussions; Magalie Duchateau (Pasteur Proteomics Platform) for help with proteomics analyses; and Denise Dorhout and Irene Rijpstra (NIOZ) for lipid analysis. This work was supported by the Agence National de la Recherche program BLANC, projects “REPVIR” and “EXOVIR.” T.M. was supported also by Bourse du Gouvernement Français (Dossier 2008661) and Allocations Pasteur-Weizmann.

Supporting Information

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 113 | No. 9
March 1, 2016
PubMed: 26884161

Classifications

Data Availability

Data deposition: The sequence reported in this paper has been deposited in the GenBank database (accession no. KU307456).

Submission history

Published online: February 16, 2016
Published in issue: March 1, 2016

Keywords

  1. hyperthermophilic archaea
  2. virion organization
  3. filamentous viruses

Acknowledgments

We thank Mery Pina for help in collecting environmental samples; Soizick Lucas-Staat and Jérémie Chaligné for assistance in experiments; Patrick Forterre for helpful discussions; Magalie Duchateau (Pasteur Proteomics Platform) for help with proteomics analyses; and Denise Dorhout and Irene Rijpstra (NIOZ) for lipid analysis. This work was supported by the Agence National de la Recherche program BLANC, projects “REPVIR” and “EXOVIR.” T.M. was supported also by Bourse du Gouvernement Français (Dossier 2008661) and Allocations Pasteur-Weizmann.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Elena Ilka Rensen1
Department of Microbiology, Institut Pasteur, 75015 Paris, France;
Tomohiro Mochizuki1
Department of Microbiology, Institut Pasteur, 75015 Paris, France;
Earth-Life Science Institute, Tokyo Institute of Technology, Tokyo 152-8550, Japan;
Emmanuelle Quemin
Department of Microbiology, Institut Pasteur, 75015 Paris, France;
Stefan Schouten
Department of Marine Organic Biogeochemistry, Royal Netherlands Institute for Sea Research, 1790 AB Den Burg, The Netherlands
Mart Krupovic2 [email protected]
Department of Microbiology, Institut Pasteur, 75015 Paris, France;
David Prangishvili2 [email protected]
Department of Microbiology, Institut Pasteur, 75015 Paris, France;

Notes

2
To whom correspondence may be addressed. Email: [email protected] or [email protected].
Author contributions: E.I.R., T.M., M.K., and D.P. designed research; E.I.R., T.M., E.Q., and S.S. performed research; E.I.R., T.M., S.S., M.K., and D.P. analyzed data; and M.K. and D.P. wrote the paper.
1
E.I.R. and T.M. contributed equally to this work.

Competing Interests

The authors declare no conflict of interest.

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    A virus of hyperthermophilic archaea with a unique architecture among DNA viruses
    Proceedings of the National Academy of Sciences
    • Vol. 113
    • No. 9
    • pp. 2319-E1328

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