Letter

Nature 455, 100-104 (4 September 2008) | doi:10.1038/nature07218; Received 16 June 2008; Accepted 27 June 2008; Published online 6 August 2008

The virophage as a unique parasite of the giant mimivirus

Bernard La Scola1,6, Christelle Desnues1,6, Isabelle Pagnier1, Catherine Robert1, Lina Barrassi1, Ghislain Fournous1, Michèle Merchat2, Marie Suzan-Monti1, Patrick Forterre3,4, Eugene Koonin5 & Didier Raoult1

  1. URMITE, Centre National de la Recherche Scientifique UMR IRD 6236, Faculté de Médecine, Université de la Méditerranée, 27 Boulevard Jean Moulin, 13385 Marseille Cedex 5, France
  2. Climespace, 185 Rue de Bercy, 75012 Paris, France
  3. Biologie Moléculaire du Gène chez les Extrêmophiles, Institut de Génétique et Microbiologie, Bâtiment 409, Université Paris Sud, Centre d'Orsay, 91405 Orsay Cedex, France
  4. Biologie Moléculaire du Gène chez les Extrêmophiles, Département de Microbiologie, Institut Pasteur, 25 rue du Dr Roux, 75724 Paris Cedex 15, France
  5. National Center for Biotechnology Information (NCBI), National Library of Medicine, National Institutes of Health, Building 38A, Room 5N503, 8600 Rockville Pike, Bethesda, Maryland 20894, USA
  6. These authors contributed equally to this work.

Correspondence to: Didier Raoult1 Correspondence and requests for materials should be addressed to D.R. (Email: didier.raoult@gmail.com).

Viruses are obligate parasites of Eukarya, Archaea and Bacteria. Acanthamoeba polyphaga mimivirus (APMV) is the largest known virus; it grows only in amoeba and is visible under the optical microscope. Mimivirus possesses a 1,185-kilobase double-stranded linear chromosome whose coding capacity is greater than that of numerous bacteria and archaea1, 2, 3. Here we describe an icosahedral small virus, Sputnik, 50 nm in size, found associated with a new strain of APMV. Sputnik cannot multiply in Acanthamoeba castellanii but grows rapidly, after an eclipse phase, in the giant virus factory found in amoebae co-infected with APMV4. Sputnik growth is deleterious to APMV and results in the production of abortive forms and abnormal capsid assembly of the host virus. The Sputnik genome is an 18.343-kilobase circular double-stranded DNA and contains genes that are linked to viruses infecting each of the three domains of life Eukarya, Archaea and Bacteria. Of the 21 predicted protein-coding genes, eight encode proteins with detectable homologues, including three proteins apparently derived from APMV, a homologue of an archaeal virus integrase, a predicted primase–helicase, a packaging ATPase with homologues in bacteriophages and eukaryotic viruses, a distant homologue of bacterial insertion sequence transposase DNA-binding subunit, and a Zn-ribbon protein. The closest homologues of the last four of these proteins were detected in the Global Ocean Survey environmental data set5, suggesting that Sputnik represents a currently unknown family of viruses. Considering its functional analogy with bacteriophages, we classify this virus as a virophage. The virophage could be a vehicle mediating lateral gene transfer between giant viruses.

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