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Proc Natl Acad Sci USA. Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology
[Source: Proceedings of the National Academy of Sciences of the United States of America, full page: (LINK). Abstract, edited.]
Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology
Matthieu Legendre<SUP>a</SUP>,<SUP>1</SUP>, Julia Bartoli<SUP>a</SUP>,<SUP>1</SUP>, Lyubov Shmakova<SUP>b</SUP>, Sandra Jeudy<SUP>a</SUP>, Karine Labadie<SUP>c</SUP>, Annie Adrait<SUP>d</SUP>, Magali Lescot<SUP>a</SUP>, Olivier Poirot<SUP>a</SUP>, Lionel Bertaux<SUP>a</SUP>, Christophe Bruley<SUP>d</SUP>, Yohann Cout?<SUP>d</SUP>, Elizaveta Rivkina<SUP>b</SUP>, Chantal Abergel<SUP>a</SUP>,<SUP>2</SUP>, and Jean-Michel Claverie<SUP>a</SUP>,<SUP>e</SUP>,<SUP>2</SUP>
<SUP></SUP>
Author Affiliations: <SUP>a</SUP>Structural and Genomic Information Laboratory, Unit? Mixte de Recherche 7256 (Institut de Microbiologie de la M?diterran?e) Centre National de la Recherche Scientifique, Aix?Marseille Universit?, 13288 Marseille Cedex 9, France; <SUP>b</SUP>Institute of Physicochemical and Biological Problems in Soil Science, Russian Academy of Sciences, Pushchino 142290, Russia; <SUP>c</SUP>Commissariat ? l?Energie Atomique, Institut de G?nomique, Centre National de S?quen?age, 91057 Evry Cedex, France; <SUP>d</SUP>Commissariat ? l?Energie Atomique, Institut de Recherches en Technologies et Sciences pour le Vivant, Biologie ? Grande Echelle, Institut National de la Sant? et de la Recherche M?dicale, Unit? 1038, Universit? Joseph Fourier Grenoble 1, 38054 Grenoble, France; and <SUP>e</SUP>Assistance Publique - Hopitaux de Marseille, 13385 Marseille, France
Edited by James L. Van Etten, University of Nebraska?Lincoln, Lincoln, NE, and approved January 30, 2014 (received for review November 7, 2013)
Abstract
Significance
Giant DNA viruses are visible under a light microscope and their genomes encode more proteins than some bacteria or intracellular parasitic eukaryotes. There are two very distinct types and infect unicellular protists such as Acanthamoeba. On one hand, Megaviridae possess large pseudoicosahedral capsids enclosing a megabase-sized adenine?thymine-rich genome, and on the other, the recently discovered Pandoraviruses exhibit micron-sized amphora-shaped particles and guanine?cytosine-rich genomes of up to 2.8 Mb. While initiating a survey of the Siberian permafrost, we isolated a third type of giant virus combining the Pandoravirus morphology with a gene content more similar to that of icosahedral DNA viruses. This suggests that pandoravirus-like particles may correspond to an unexplored diversity of unconventional DNA virus families.
Abstract
The largest known DNA viruses infect Acanthamoeba and belong to two markedly different families. The Megaviridae exhibit pseudo-icosahedral virions up to 0.7 μm in diameter and adenine?thymine (AT)-rich genomes of up to 1.25 Mb encoding a thousand proteins. Like their Mimivirus prototype discovered 10 y ago, they entirely replicate within cytoplasmic virion factories. In contrast, the recently discovered Pandoraviruses exhibit larger amphora-shaped virions 1 μm in length and guanine?cytosine-rich genomes up to 2.8 Mb long encoding up to 2,500 proteins. Their replication involves the host nucleus. Whereas the Megaviridae share some general features with the previously described icosahedral large DNA viruses, the Pandoraviruses appear unrelated to them. Here we report the discovery of a third type of giant virus combining an even larger pandoravirus-like particle 1.5 μm in length with a surprisingly smaller 600 kb AT-rich genome, a gene content more similar to Iridoviruses and Marseillevirus, and a fully cytoplasmic replication reminiscent of the Megaviridae. This suggests that pandoravirus-like particles may be associated with a variety of virus families more diverse than previously envisioned. This giant virus, named Pithovirus sibericum, was isolated from a >30,000-y-old radiocarbon-dated sample when we initiated a survey of the virome of Siberian permafrost. The revival of such an ancestral amoeba-infecting virus used as a safe indicator of the possible presence of pathogenic DNA viruses, suggests that the thawing of permafrost either from global warming or industrial exploitation of circumpolar regions might not be exempt from future threats to human or animal health.
giant DNA virus - late Pleistocene - icosahedral capsid
Footnotes
<SUP>1</SUP>M. Legendre and J.B. contributed equally to this work.
<SUP>2</SUP>To whom correspondence may be addressed. E-mail: claverie@igs.cnrs-mrs.fr or Chantal.Abergel@igs.cnrs-mrs.fr.
Author contributions: C.A. and J.-M.C. designed research; M. Legendre, J.B., S.J., A.A., M. Lescot, L.B., C.A., and J.-M.C. performed research; K.L. performed DNA sequencing; L.S., K.L., C.B., Y.C., and E.R. contributed new reagents/analytic tools; M. Legendre, J.B., M. Lescot, O.P., Y.C., C.A., and J.-M.C. analyzed data; and M. Legendre, C.A., and J.-M.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The Pithovirus genome sequence reported in this paper has been deposited in GenBank database (accession no. KF740664). The MS proteomics data reported in this paper have been deposited in the ProteomeXchange Consortium database, http://proteomecentral.proteomexchange.org/cgi/GetDataset?ID=PXD000460, via the Proteomics Identifications database (www.ebi.ac.uk/pride/archive) partner repository [identifier no. PXD000460 (10.6019/PXD000460)].
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1320670111/-/DCSupplemental.
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Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology
Matthieu Legendre<SUP>a</SUP>,<SUP>1</SUP>, Julia Bartoli<SUP>a</SUP>,<SUP>1</SUP>, Lyubov Shmakova<SUP>b</SUP>, Sandra Jeudy<SUP>a</SUP>, Karine Labadie<SUP>c</SUP>, Annie Adrait<SUP>d</SUP>, Magali Lescot<SUP>a</SUP>, Olivier Poirot<SUP>a</SUP>, Lionel Bertaux<SUP>a</SUP>, Christophe Bruley<SUP>d</SUP>, Yohann Cout?<SUP>d</SUP>, Elizaveta Rivkina<SUP>b</SUP>, Chantal Abergel<SUP>a</SUP>,<SUP>2</SUP>, and Jean-Michel Claverie<SUP>a</SUP>,<SUP>e</SUP>,<SUP>2</SUP>
<SUP></SUP>
Author Affiliations: <SUP>a</SUP>Structural and Genomic Information Laboratory, Unit? Mixte de Recherche 7256 (Institut de Microbiologie de la M?diterran?e) Centre National de la Recherche Scientifique, Aix?Marseille Universit?, 13288 Marseille Cedex 9, France; <SUP>b</SUP>Institute of Physicochemical and Biological Problems in Soil Science, Russian Academy of Sciences, Pushchino 142290, Russia; <SUP>c</SUP>Commissariat ? l?Energie Atomique, Institut de G?nomique, Centre National de S?quen?age, 91057 Evry Cedex, France; <SUP>d</SUP>Commissariat ? l?Energie Atomique, Institut de Recherches en Technologies et Sciences pour le Vivant, Biologie ? Grande Echelle, Institut National de la Sant? et de la Recherche M?dicale, Unit? 1038, Universit? Joseph Fourier Grenoble 1, 38054 Grenoble, France; and <SUP>e</SUP>Assistance Publique - Hopitaux de Marseille, 13385 Marseille, France
Edited by James L. Van Etten, University of Nebraska?Lincoln, Lincoln, NE, and approved January 30, 2014 (received for review November 7, 2013)
Abstract
Significance
Giant DNA viruses are visible under a light microscope and their genomes encode more proteins than some bacteria or intracellular parasitic eukaryotes. There are two very distinct types and infect unicellular protists such as Acanthamoeba. On one hand, Megaviridae possess large pseudoicosahedral capsids enclosing a megabase-sized adenine?thymine-rich genome, and on the other, the recently discovered Pandoraviruses exhibit micron-sized amphora-shaped particles and guanine?cytosine-rich genomes of up to 2.8 Mb. While initiating a survey of the Siberian permafrost, we isolated a third type of giant virus combining the Pandoravirus morphology with a gene content more similar to that of icosahedral DNA viruses. This suggests that pandoravirus-like particles may correspond to an unexplored diversity of unconventional DNA virus families.
Abstract
The largest known DNA viruses infect Acanthamoeba and belong to two markedly different families. The Megaviridae exhibit pseudo-icosahedral virions up to 0.7 μm in diameter and adenine?thymine (AT)-rich genomes of up to 1.25 Mb encoding a thousand proteins. Like their Mimivirus prototype discovered 10 y ago, they entirely replicate within cytoplasmic virion factories. In contrast, the recently discovered Pandoraviruses exhibit larger amphora-shaped virions 1 μm in length and guanine?cytosine-rich genomes up to 2.8 Mb long encoding up to 2,500 proteins. Their replication involves the host nucleus. Whereas the Megaviridae share some general features with the previously described icosahedral large DNA viruses, the Pandoraviruses appear unrelated to them. Here we report the discovery of a third type of giant virus combining an even larger pandoravirus-like particle 1.5 μm in length with a surprisingly smaller 600 kb AT-rich genome, a gene content more similar to Iridoviruses and Marseillevirus, and a fully cytoplasmic replication reminiscent of the Megaviridae. This suggests that pandoravirus-like particles may be associated with a variety of virus families more diverse than previously envisioned. This giant virus, named Pithovirus sibericum, was isolated from a >30,000-y-old radiocarbon-dated sample when we initiated a survey of the virome of Siberian permafrost. The revival of such an ancestral amoeba-infecting virus used as a safe indicator of the possible presence of pathogenic DNA viruses, suggests that the thawing of permafrost either from global warming or industrial exploitation of circumpolar regions might not be exempt from future threats to human or animal health.
giant DNA virus - late Pleistocene - icosahedral capsid
Footnotes
<SUP>1</SUP>M. Legendre and J.B. contributed equally to this work.
<SUP>2</SUP>To whom correspondence may be addressed. E-mail: claverie@igs.cnrs-mrs.fr or Chantal.Abergel@igs.cnrs-mrs.fr.
Author contributions: C.A. and J.-M.C. designed research; M. Legendre, J.B., S.J., A.A., M. Lescot, L.B., C.A., and J.-M.C. performed research; K.L. performed DNA sequencing; L.S., K.L., C.B., Y.C., and E.R. contributed new reagents/analytic tools; M. Legendre, J.B., M. Lescot, O.P., Y.C., C.A., and J.-M.C. analyzed data; and M. Legendre, C.A., and J.-M.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The Pithovirus genome sequence reported in this paper has been deposited in GenBank database (accession no. KF740664). The MS proteomics data reported in this paper have been deposited in the ProteomeXchange Consortium database, http://proteomecentral.proteomexchange.org/cgi/GetDataset?ID=PXD000460, via the Proteomics Identifications database (www.ebi.ac.uk/pride/archive) partner repository [identifier no. PXD000460 (10.6019/PXD000460)].
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1320670111/-/DCSupplemental.
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