The virophage as a unique parasite of the giant mimivirus (original) (raw)

Nature volume 455, pages 100–104 (2008)Cite this article

Abstract

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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Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

The virophage genome has been deposited in GenBank under accession number EU606015. The Acanthamoeba castellanii mamavirus genes with homologues found in the Sputnik genome have been deposited in GenBank under accession numbers EU827539, EU827540 and EU827541.

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Acknowledgements

We thank X. de Lamballerie, S. Azza, P. de Clocquement, L. Espinosa, B. Campagna, N. Aldrovandi, V. Brice, A. Bernard, C. Ivars, B. Giumelli and Y. Wolf for expert assistance. This work was funded by the Centre National de la Recherche Scientifique (CNRS, crédits récurrents). I.P. is funded by a CIFFRE fellowship, E.K. is supported by the Intramural Research Program of the National Institutes of Health, National Library of Medicine, and P.F. is funded by the Institut Universitaire de France.

Author contributions D.R. and B.L.S. supervised the project and wrote the manuscript. C.D., P.F. and E.K. contributed to sequence analysis, interpretation of the results and writing of the manuscript. I.P. isolated the virus. M.S.-M. contributed to viral cycle analysis, interpretation of the results and writing of the manuscript. M.M. provided water samples. L.B. conducted the viral cycle experiment. C.R. and G.F. sequenced the genome.

Author information

Author notes

  1. Bernard La Scola and Christelle Desnues: These authors contributed equally to this work.

Authors and Affiliations

  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 ,
    Bernard La Scola, Christelle Desnues, Isabelle Pagnier, Catherine Robert, Lina Barrassi, Ghislain Fournous, Marie Suzan-Monti & Didier Raoult
  2. Climespace, 185 Rue de Bercy, 75012 Paris, France ,
    Michèle Merchat
  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 ,
    Patrick Forterre
  4. Département de Microbiologie, Biologie Moléculaire du Gène chez les Extrêmophiles, Institut Pasteur, 25 rue du Dr Roux, 75724 Paris Cedex 15, France,
    Patrick Forterre
  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 ,
    Eugene Koonin

Authors

  1. Bernard La Scola
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  2. Christelle Desnues
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  3. Isabelle Pagnier
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  4. Catherine Robert
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  5. Lina Barrassi
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  6. Ghislain Fournous
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  7. Michèle Merchat
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  8. Marie Suzan-Monti
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  9. Patrick Forterre
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  10. Eugene Koonin
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  11. Didier Raoult
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Corresponding author

Correspondence toDidier Raoult.

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La Scola, B., Desnues, C., Pagnier, I. et al. The virophage as a unique parasite of the giant mimivirus.Nature 455, 100–104 (2008). https://doi.org/10.1038/nature07218

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Editorial Summary

The biter BIT: Viral infections for viruses

The first 'giant virus' isolate came from a cooling tower in Bradford, UK. Initially mistaken for a bacterium because of its size — three times larger than that of the biggest known viruses and bigger than many bacteria — it was found in the protozoon Acanthamoeba polyphaga. It was termed a mimivirus (for mimicking microbe) and became known as APMV (Acanthamoeba polyphaga mimivirus). Now an even larger APMV strain, a 'mamavirus', has been isolated from a water cooling tower in Paris. Remarkably it is not alone, but is itself parasitized by a 'satellite virus'. Called Sputnik, it replicates in the virus factory built in amoebae co-infected with APMV. By analogy with bacteriophage, Sputnik is seen as the first virophage to be discovered. It may be the tip of a virophage iceberg, since metagenomic studies of ocean waters reveal an abundance of genetic sequences closely related to giant viruses, leading to a suspicion that they are a common parasite of plankton.