Unpacking the Baggage: Origin and Evolution of Giant Viruses

  • Jonathan FiléeEmail author
  • Michael Chandler


Giant viruses (GVs) form a diverse group of virus that all belong to the Nucleo Cytoplasmic Large DNA virus (NCLDV) family. They infects a wide range of eukaryotic hosts (for example, vertebrates, insects, protists,…) and also show a huge range in genome size (between 100 kb and 1.2 Mb). Here we review some recent results that shed light on the origin and genome evolution of these viruses with a specific emphasis on the nature of their relationships with cellular organisms. We show that genome gigantism is explained by gene transfers and gene duplication and do not result from genome reduction from a cellular ancestors. We discuss the importance of mobile genetic elements, the role of ORFans during GV evolution and propose that the evolutionary success of GV is intimately link to the extreme plasticity of their genomes. Finally we speculate about the different scenario that explain GV origins and argue that GVs probably emerge from simple genetic elements followed by multiple waves of genomic expansion/simplification.


Core Gene Lateral Gene Transfer Gene Acquisition Giant Virus Paralogous Family 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Andersson SG, Zomorodipour A et al (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396(6707):133–140PubMedCrossRefGoogle Scholar
  2. Arslan D, Legendre M et al (2011) Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci USA 108(42):17486–17491PubMedCrossRefGoogle Scholar
  3. Benarroch D, Claverie JM et al (2006) Characterization of mimivirus DNA topoisomerase IB suggests horizontal gene transfer between eukaryal viruses and bacteria. J Virol 80(1):314–321PubMedCrossRefGoogle Scholar
  4. Boyer M, Yutin N et al (2009) Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms. Proc Natl Acad Sci USA 106(51):21848–21853PubMedCrossRefGoogle Scholar
  5. Boyer M, Gimenez G et al (2010a) Classification and determination of possible origins of ORFans through analysis of nucleocytoplasmic large DNA viruses. Intervirology 53(5):310–320PubMedCrossRefGoogle Scholar
  6. Boyer M, Madoui MA et al (2010b) Phylogenetic and phyletic studies of informational genes in genomes highlight existence of a 4 domain of life including giant viruses. PLoS One 5(12):e15530PubMedCrossRefGoogle Scholar
  7. Boyer M, Azza S et al (2011) Mimivirus shows dramatic genome reduction after intraamoebal culture. Proc Natl Acad Sci USA 108(25):10296–10301PubMedCrossRefGoogle Scholar
  8. Claverie JM (2006) Viruses take center stage in cellular evolution. Genome Biol 7(6):110PubMedCrossRefGoogle Scholar
  9. Colson P, Yutin N et al (2011) Viruses with more than 1,000 genes: Mamavirus, a new Acanthamoeba polyphaga mimivirus strain, and reannotation of Mimivirus genes. Genome Biol Evol 3:737–742PubMedCrossRefGoogle Scholar
  10. Evans DH, Stuart D et al (1988) High levels of genetic recombination among cotransfected plasmid DNAs in poxvirus-infected mammalian cells. J Virol 62(2):367–375PubMedGoogle Scholar
  11. Filee J, Chandler M (2008) Convergent mechanisms of genome evolution of large and giant DNA viruses. Res Microbiol 159(5):325–331PubMedCrossRefGoogle Scholar
  12. Filee J, Chandler M (2010) Gene exchange and the origin of giant viruses. Intervirology 53(5):354–361PubMedCrossRefGoogle Scholar
  13. Filee J, Tetart F et al (2005) Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere. Proc Natl Acad Sci USA 102(35):12471–12476PubMedCrossRefGoogle Scholar
  14. Filee J, Siguier P et al (2007) I am what I eat and I eat what I am: acquisition of bacterial genes by giant viruses. Trends Genet 23(1):10–15PubMedCrossRefGoogle Scholar
  15. Filee J, Pouget N et al (2008) Phylogenetic evidence for extensive lateral acquisition of cellular genes by nucleocytoplasmic large DNA viruses. BMC Evol Biol 8:320PubMedCrossRefGoogle Scholar
  16. Fischer MG, Suttle CA (2011) A virophage at the origin of large DNA transposons. Science 332(6026):231–234PubMedCrossRefGoogle Scholar
  17. Fischer MG, Allen MJ et al (2010) Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci USA 107(45):19508–19513PubMedCrossRefGoogle Scholar
  18. Forterre P (2010) Giant viruses: conflicts in revisiting the virus concept. Intervirology 53(5):362–378PubMedCrossRefGoogle Scholar
  19. Iyer LM, Balaji S et al (2006) Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 117(1):156–184PubMedCrossRefGoogle Scholar
  20. Katinka MD, Duprat S et al (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414(6862):450–453PubMedCrossRefGoogle Scholar
  21. Koonin EV, Yutin N (2010) Origin and evolution of eukaryotic large nucleo-cytoplasmic DNA viruses. Intervirology 53(5):284–292PubMedCrossRefGoogle Scholar
  22. Kristensen DM, Mushegian AR et al (2010) New dimensions of the virus world discovered through metagenomics. Trends Microbiol 18(1):11–19PubMedCrossRefGoogle Scholar
  23. Krupovic M, Bamford DH (2008) Virus evolution: how far does the double beta-barrel viral lineage extend? Nat Rev Microbiol 6(12):941–948PubMedCrossRefGoogle Scholar
  24. La Scola B, Desnues C et al (2008) The virophage as a unique parasite of the giant mimivirus. Nature 455(7209):100–104PubMedCrossRefGoogle Scholar
  25. Monier A, Claverie JM et al (2008) Taxonomic distribution of large DNA viruses in the sea. Genome Biol 9(7):R106PubMedCrossRefGoogle Scholar
  26. Monier A, Pagarete A et al (2009) Horizontal gene transfer of an entire metabolic pathway between a eukaryotic alga and its DNA virus. Genome Res 19(8):1441–1449PubMedCrossRefGoogle Scholar
  27. Moreira D, Brochier-Armanet C (2008) Giant viruses, giant chimeras: the multiple evolutionary histories of mimivirus genes. BMC Evol Biol 8:12PubMedCrossRefGoogle Scholar
  28. Moreira D, Lopez-Garcia P (2005) “Comment on ”the 1.2-Megabase genome sequence of mimivirus. Science 308(5725):1114, author reply 1114PubMedCrossRefGoogle Scholar
  29. Mosig G, Gewin J et al (2001) Two recombination-dependent DNA replication pathways of bacteriophage T4, and their roles in mutagenesis and horizontal gene transfer. Proc Natl Acad Sci USA 98(15):8306–8311PubMedCrossRefGoogle Scholar
  30. Nagasaki K, Tomaru Y et al (2003) Growth characteristics and intraspecies host specificity of a large virus infecting the dinoflagellate Heterocapsa circularisquama. Appl Environ Microbiol 69(5):2580–2586PubMedCrossRefGoogle Scholar
  31. Prangishvili D, Stedman K et al (2001) Viruses of the extremely thermophilic archaeon Sulfolobus. Trends Microbiol 9(1):39–43PubMedCrossRefGoogle Scholar
  32. Raoult D, Audic S et al (2004) The 1.2-Megabase genome sequence of mimivirus. Science 306(5700):1344–1350PubMedCrossRefGoogle Scholar
  33. Reuven NB, Antoku S et al (2004) The UL12.5 Gene product of herpes simplex virus type 1 exhibits nuclease and strand exchange activities but does not localize to the nucleus. J Virol 78(9):4599–4608PubMedCrossRefGoogle Scholar
  34. Sogayar MI, Gregorio EA (1986) Cytoplasmic inclusions in Giardia: an electron microscopy study. Ann Trop Med Parasitol 80(1):49–52PubMedGoogle Scholar
  35. Stenzel DJ, Boreham PF (1997) Virus-like particles in Blastocystis sp. From simian faecal material. Int J Parasitol 27(3):345–348PubMedCrossRefGoogle Scholar
  36. Suhre K (2005) Gene and genome duplication in Acanthamoeba polyphaga mimivirus. J Virol 79(22):14095–14101PubMedCrossRefGoogle Scholar
  37. Tessman I (1985) Genetic recombination of the DNA plant virus PBCV-1 in a chlorella-like alga. Virology 145:319–322PubMedCrossRefGoogle Scholar
  38. Thomas V, Greub G (2010) Amoeba/amoebal symbiont genetic transfers: lessons from giant virus neighbours. Intervirology 53(5):254–267PubMedCrossRefGoogle Scholar
  39. Van Etten JL, Meints RH (1999) Giant viruses infecting algae. Annu Rev Microbiol 53:447–494PubMedCrossRefGoogle Scholar
  40. Weynberg KD, Allen MJ et al (2011) Genome sequence of Ostreococcus tauri virus OtV-2 throws light on the role of picoeukaryote niche separation in the ocean. J Virol 85(9):4520–4529PubMedCrossRefGoogle Scholar
  41. Williams TA, Embley TM et al (2011) Informational gene phylogenies do not support a fourth domain of life for nucleocytoplasmic large DNA viruses. PLoS One 6(6):e21080PubMedCrossRefGoogle Scholar
  42. Wilson WH, Van Etten JL et al (2009) The phycodnaviridae: the story of how tiny giants rule the world. Curr Top Microbiol Immunol 328:1–42PubMedCrossRefGoogle Scholar
  43. Yau S, Lauro FM et al (2011) Virophage control of Antarctic algal host-virus dynamics. Proc Natl Acad Sci USA 108(15):6163–6168PubMedCrossRefGoogle Scholar
  44. Yutin N, Wolf YI et al (2009) Eukaryotic large nucleo-cytoplasmic DNA viruses: clusters of orthologous genes and reconstruction of viral genome evolution. Virol J 6:223PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Laboratoire Evolution, Génomes et SpéciationCNRS UPR 9034Gif sur Yvette CedexFrance
  2. 2.Laboratoire de Microbiologie et Génétique MoléculaireCNRS UMR 5100Toulouse Cedex 04France

Personalised recommendations