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Vol. 53, No. 5, 2010
Issue release date: June 2010
Section title: Paper
Free Access
Intervirology 2010;53:284–292

Origin and Evolution of Eukaryotic Large Nucleo-Cytoplasmic DNA Viruses

Koonin E.V. · Yutin N.
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Md., USA
email Corresponding Author

Eugene V. Koonin

National Center for Biotechnology Information

National Library of Medicine, National Institutes of Health

Bethesda, MD 20894 (USA)



  1. Raoult D, Forterre P: Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol 2008;6:315–319.
  2. Forterre P: The origin of viruses and their possible roles in major evolutionary transitions. Virus Res 2006;117:5–16.
  3. Koonin EV, Senkevich TG, Dolja VV: The ancient virus world and evolution of cells. Biol Direct 2006;1:29.
  4. Iyer LM, Aravind L, Koonin EV: Common origin of four diverse families of large eukaryotic DNA viruses. J Virol 2001;75:11720–11734.
  5. Iyer LM, Balaji S, Koonin EV, Aravind L: Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 2006;117:156–184.
  6. Moss B: Poxviridae: the viruses and their replication; in Fields BN, Knipe DM, Howley PM, Griffin DE (eds): Fields Virology. Philadelphia, Lippincott, Williams & Wilkins, 2001, vol 2, pp 2849–2884.
  7. Lefkowitz EJ, Wang C, Upton C: Poxviruses: past, present and future. Virus Res 2006;117:105–118.
  8. Hughes AL, Irausquin S, Friedman R: The evolutionary biology of poxviruses. Infect Genet Evol 2010;10:50–59.
  9. La Scola B, Desnues C, Pagnier I, Robert C, Barrassi L, Fournous G, Merchat M, Suzan-Monti M, Forterre P, Koonin E, Raoult D: The virophage as a unique parasite of the giant Mimivirus. Nature 2008;455:100–104.
  10. Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, La Scola B, Suzan M, Claverie JM: The 1.2-megabase genome sequence of Mimivirus. Science 2004;306:1344–1350.
  11. Claverie JM, Abergel C: Mimivirus and its virophage. Annu Rev Genet 2009;43:49–66.
  12. Claverie JM, Abergel C, Ogata H: Mimivirus. Curr Top Microbiol Immunol 2009;328:89–121.
  13. Suzan-Monti M, La Scola B, Raoult D: Genomic and evolutionary aspects of Mimivirus. Virus Res 2006;117:145–155.
  14. Van Etten JL: Unusual life style of giant chlorella viruses. Annu Rev Genet 2003;37:153–195.
  15. Yutin N, Wolf YI, Raoult D, Koonin EV: Eukaryotic large nucleo-cytoplasmic DNA viruses: Clusters of orthologous genes and reconstruction of viral genome evolution. Virol J 2010;6:223.

    External Resources

  16. Boyer M, Yutin N, Pagnier I, Barrassi L, Fournous G, Espinosa M, Robert C, Azza A, Sun S, Rossmann MG, Suzan-Monti M, La Scola B, Koonin EV, Raoult D: Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimaeric microorganisms. Proc Natl Acad Sci USA 2009;106:21848–21853.
  17. Koonin EV: Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 2003;1:127–136.
  18. Charlebois RL, Doolittle WF: Computing prokaryotic gene ubiquity: rescuing the core from extinction. Genome Res 2004;14:2469–2477.
  19. Wolf YI, Rogozin IB, Grishin NV, Koonin EV: Genome trees and the tree of life. Trends Genet 2002;18:472–479.
  20. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ, Gray MW: The tree of eukaryotes. Trends Ecol Evol 2005;20:670–676.
  21. Keeling PJ: Genomics: deep questions in the tree of life. Science 2007;317:1875–1876.
  22. Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AG, Roger AJ: Phylogenomic analyses support the monophyly of excavata and resolve relationships among eukaryotic ‘Supergroups’. Proc Natl Acad Sci USA 2009;106:3859–3864.
  23. Monier A, Claverie JM, Ogata H: Taxonomic distribution of large DNA viruses in the sea. Genome Biol 2008;9:R106.
  24. Monier A, Larsen JB, Sandaa RA, Bratbak G, Claverie JM, Ogata H: Marine Mimivirus relatives are probably large algal viruses. Virol J 2008;5:12.
  25. Kristensen DM, Mushegian AR, Dolja VV, Koonin EV: New dimensions of the virus world discovered through metagenomics. Trends Microbiol 2010;18:11–19.
  26. Ogata H, Toyoda K, Tomaru Y, Nakayama N, Shirai Y, Claverie JM, Nagasaki K: Remarkable sequence similarity between the dinoflagellate-infecting marine girus and the terrestrial pathogen African swine fever virus. Virol J 2009;6:178.
  27. Csuros M, Miklos I: Streamlining and large ancestral genomes in archaea inferred with a phylogenetic birth-and-death model. Mol Biol Evol 2009;26:2087–2095.
  28. Koonin EV, Mushegian AR, Bork P: Non-orthologous gene displacement. Trends Genet 1996;12:334–336.
  29. Yutin N, Koonin EV: Evolution of DNA ligases of nucleo-cytoplasmic large DNA viruses of eukaryotes: a case of hidden complexity. Biol Direct 2009;4:51.
  30. Paran N, De Silva FS, Senkevich TG, Moss B: Recruitment of cellular DNA ligase I to cytoplasmic vaccinia virus factories complements viral DNA replication in the absence of the viral ligase. Cell Host Microbe 2009;6:563–569.
  31. Claverie JM, Grzela R, Lartigue A, Bernadac A, Nitsche S, Vacelet J, Ogata H, Abergel C: Mimivirus and Mimiviridae: giant viruses with an increasing number of potential hosts, including corals and sponges. J Invertebr Pathol 2009;101:172–180.
  32. Filee J, Pouget N, Chandler M: Phylogenetic evidence for extensive lateral acquisition of cellular genes by nucleocytoplasmic large DNA viruses. BMC Evol Biol 2008;8:320.
  33. Filee J, Siguier P, Chandler M: I am what I eat and I eat what I am: acquisition of bacterial genes by giant viruses. Trends Genet 2007;23:10–15.
  34. Makarova KS, Wolf YI, Mekhedov SL, Mirkin BG, Koonin EV: Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell. Nucleic Acids Res 2005;33:4626–4638.
  35. Podell S, Gaasterland T: DarkHorse: a method for genome-wide prediction of horizontal gene transfer. Genome Biol 2007;8:R16.
  36. Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, Canese K, Chetvernin V, Church DM, Dicuccio M, Federhen S, Feolo M, Geer LY, Helmberg W, Kapustin Y, Landsman D, Lipman DJ, Lu Z, Madden TL, Madej T, Maglott DR, Marchler-Bauer A, Miller V, Mizrachi I, Ostell J, Panchenko A, Pruitt KD, Schuler GD, Sequeira E, Sherry ST, Shumway M, Sirotkin K, Slotta D, Souvorov A, Starchenko G, Tatusova TA, Wagner L, Wang Y, John Wilbur W, Yaschenko E, Ye J: Database resources of the national center for biotechnology information. Nucleic Acids Res 2010;38(Database issue):D5–D16.
  37. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389–3402.
  38. Altschul SF, Koonin EV: PSI-BLAST: a tool for making discoveries in sequence databases. Trends Biochem Sci 1998;23:444–447.
  39. Iyer LM, Koonin EV, Aravind L: Extensive domain shuffling in transcription regulators of DNA viruses and implications for the origin of fungal apses transcription factors. Genome Biol 2002;3:RESEARCH0012.

    External Resources

  40. Iyer LM, Makarova KS, Koonin EV, Aravind L: Comparative genomics of the FTSK-HERA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res 2004;32:5260–5279.
  41. Garcia AD, Aravind L, Koonin EV, Moss B: Bacterial-type DNA Holliday junction resolvases in eukaryotic viruses. Proc Natl Acad Sci USA 2000;97:8926–8931.