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Research Article

Genome of Phaeocystis globosa virus PgV-16T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes

Sebastien Santini, Sandra Jeudy, Julia Bartoli, Olivier Poirot, Magali Lescot, Chantal Abergel, Valérie Barbe, K. Eric Wommack, Anna A. M. Noordeloos, Corina P. D. Brussaard, and Jean-Michel Claverie
  1. aStructural and Genomic Information Laboratory, Unité Mixte de Recherche 7256, Centre National de la Recherche Scientifique, Aix-Marseille Université, 13288 Marseille Cedex 9, France;
  2. bCommissariat à l’Energie Atomique–Institut de Génomique, 91057 Evry Cedex, France;
  3. cDepartment of Plant and Soil Sciences, University of Delaware, Newark, DE 19711;
  4. dDepartment of Biological Oceanography, Royal Netherlands Institute for Sea Research, NL-1790 AB Den Burg (Texel), The Netherlands;
  5. eAquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands; and
  6. fService de Santé Publique et d'Information Médicale, Hôpital de la Timone, Assistance Publique–Hôpitaux de Marseille, FR-13385 Marseille, France

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PNAS first published June 10, 2013; https://doi.org/10.1073/pnas.1303251110
Sebastien Santini
aStructural and Genomic Information Laboratory, Unité Mixte de Recherche 7256, Centre National de la Recherche Scientifique, Aix-Marseille Université, 13288 Marseille Cedex 9, France;
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Sandra Jeudy
aStructural and Genomic Information Laboratory, Unité Mixte de Recherche 7256, Centre National de la Recherche Scientifique, Aix-Marseille Université, 13288 Marseille Cedex 9, France;
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Julia Bartoli
aStructural and Genomic Information Laboratory, Unité Mixte de Recherche 7256, Centre National de la Recherche Scientifique, Aix-Marseille Université, 13288 Marseille Cedex 9, France;
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Olivier Poirot
aStructural and Genomic Information Laboratory, Unité Mixte de Recherche 7256, Centre National de la Recherche Scientifique, Aix-Marseille Université, 13288 Marseille Cedex 9, France;
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Magali Lescot
aStructural and Genomic Information Laboratory, Unité Mixte de Recherche 7256, Centre National de la Recherche Scientifique, Aix-Marseille Université, 13288 Marseille Cedex 9, France;
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Chantal Abergel
aStructural and Genomic Information Laboratory, Unité Mixte de Recherche 7256, Centre National de la Recherche Scientifique, Aix-Marseille Université, 13288 Marseille Cedex 9, France;
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Valérie Barbe
bCommissariat à l’Energie Atomique–Institut de Génomique, 91057 Evry Cedex, France;
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K. Eric Wommack
cDepartment of Plant and Soil Sciences, University of Delaware, Newark, DE 19711;
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Anna A. M. Noordeloos
dDepartment of Biological Oceanography, Royal Netherlands Institute for Sea Research, NL-1790 AB Den Burg (Texel), The Netherlands;
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Corina P. D. Brussaard
dDepartment of Biological Oceanography, Royal Netherlands Institute for Sea Research, NL-1790 AB Den Burg (Texel), The Netherlands;
eAquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands; and
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  • For correspondence: corina.brussaard@nioz.nl Jean-Michel.Claverie@univ-amu.fr
Jean-Michel Claverie
aStructural and Genomic Information Laboratory, Unité Mixte de Recherche 7256, Centre National de la Recherche Scientifique, Aix-Marseille Université, 13288 Marseille Cedex 9, France;
fService de Santé Publique et d'Information Médicale, Hôpital de la Timone, Assistance Publique–Hôpitaux de Marseille, FR-13385 Marseille, France
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  • For correspondence: corina.brussaard@nioz.nl Jean-Michel.Claverie@univ-amu.fr
  1. Edited by James L. Van Etten, University of Nebraska, Lincoln, NE, and approved May 1, 2013 (received for review February 22, 2013)

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Abstract

Large dsDNA viruses are involved in the population control of many globally distributed species of eukaryotic phytoplankton and have a prominent role in bloom termination. The genus Phaeocystis (Haptophyta, Prymnesiophyceae) includes several high-biomass-forming phytoplankton species, such as Phaeocystis globosa, the blooms of which occur mostly in the coastal zone of the North Atlantic and the North Sea. Here, we report the 459,984-bp-long genome sequence of P. globosa virus strain PgV-16T, encoding 434 proteins and eight tRNAs and, thus, the largest fully sequenced genome to date among viruses infecting algae. Surprisingly, PgV-16T exhibits no phylogenetic affinity with other viruses infecting microalgae (e.g., phycodnaviruses), including those infecting Emiliania huxleyi, another ubiquitous bloom-forming haptophyte. Rather, PgV-16T belongs to an emerging clade (the Megaviridae) clustering the viruses endowed with the largest known genomes, including Megavirus, Mimivirus (both infecting acanthamoeba), and a virus infecting the marine microflagellate grazer Cafeteria roenbergensis. Seventy-five percent of the best matches of PgV-16T–predicted proteins correspond to two viruses [Organic Lake phycodnavirus (OLPV)1 and OLPV2] from a hypersaline lake in Antarctica (Organic Lake), the hosts of which are unknown. As for OLPVs and other Megaviridae, the PgV-16T sequence data revealed the presence of a virophage-like genome. However, no virophage particle was detected in infected P. globosa cultures. The presence of many genes found only in Megaviridae in its genome and the presence of an associated virophage strongly suggest that PgV-16T shares a common ancestry with the largest known dsDNA viruses, the host range of which already encompasses the earliest diverging branches of domain Eukarya.

  • giant virus
  • core gene
  • gene duplication
  • mobile element
  • horizontal gene transfer

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: corina.brussaard{at}nioz.nl or Jean-Michel.Claverie{at}univ-amu.fr.
  • Author contributions: K.E.W., C.P.D.B., and J.-M.C. designed research; S.S., S.J., J.B., V.B., A.A.M.N., and C.P.D.B. performed research; S.S., S.J., O.P., M.L., C.A., and J.-M.C. analyzed data; and S.S., C.P.D.B., and J.-M.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KC662249–KC662250).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1303251110/-/DCSupplemental.

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Genome sequence of P. globosa virus PgV-16T
Sebastien Santini, Sandra Jeudy, Julia Bartoli, Olivier Poirot, Magali Lescot, Chantal Abergel, Valérie Barbe, K. Eric Wommack, Anna A. M. Noordeloos, Corina P. D. Brussaard, Jean-Michel Claverie
Proceedings of the National Academy of Sciences Jun 2013, 201303251; DOI: 10.1073/pnas.1303251110

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Genome sequence of P. globosa virus PgV-16T
Sebastien Santini, Sandra Jeudy, Julia Bartoli, Olivier Poirot, Magali Lescot, Chantal Abergel, Valérie Barbe, K. Eric Wommack, Anna A. M. Noordeloos, Corina P. D. Brussaard, Jean-Michel Claverie
Proceedings of the National Academy of Sciences Jun 2013, 201303251; DOI: 10.1073/pnas.1303251110
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