Skip to main content
Log in

“Megavirales”, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The nucleocytoplasmic large DNA viruses (NCLDVs) comprise a monophyletic group of viruses that infect animals and diverse unicellular eukaryotes. The NCLDV group includes the families Poxviridae, Asfarviridae, Iridoviridae, Ascoviridae, Phycodnaviridae, Mimiviridae and the proposed family “Marseilleviridae”. The family Mimiviridae includes the largest known viruses, with genomes in excess of one megabase, whereas the genome size in the other NCLDV families varies from 100 to 400 kilobase pairs. Most of the NCLDVs replicate in the cytoplasm of infected cells, within so-called virus factories. The NCLDVs share a common ancient origin, as demonstrated by evolutionary reconstructions that trace approximately 50 genes encoding key proteins involved in viral replication and virion formation to the last common ancestor of all these viruses. Taken together, these characteristics lead us to propose assigning an official taxonomic rank to the NCLDVs as the order “Megavirales”, in reference to the large size of the virions and genomes of these viruses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Iyer LM, Aravind L, Koonin EV (2001) Common origin of four diverse families of large eukaryotic DNA viruses. J Virol 75:11720–11734. doi:10.1128/JVI.75.23.11720-11734.2001

    Article  PubMed  CAS  Google Scholar 

  2. Iyer LM, Balaji S, Koonin EV, Aravind L (2006) Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 117:156–184. doi:10.1016/j.virusres.2006.01.009

    Article  PubMed  CAS  Google Scholar 

  3. Yutin N, Wolf YI, Raoult D, Koonin EV (2009) Eukaryotic large nucleo-cytoplasmic DNA viruses: clusters of orthologous genes and reconstruction of viral genome evolution. Virol J 6:223. doi:10.1186/1743-422X-6-223

    Article  PubMed  Google Scholar 

  4. Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, La Scola B, Suzan M, Claverie JM (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306:1344–1350. doi:10.1126/science.1101485

    Article  PubMed  CAS  Google Scholar 

  5. Claverie JM, Abergel C, Ogata H (2009) Mimivirus. Curr Top Microbiol Immunol 328:89–121

    Article  PubMed  CAS  Google Scholar 

  6. La Scola B, Campocasso A, N’Dong R, Fournous G, Barrassi L, Flaudrops C, Raoult D (2010) Tentative characterization of new environmental giant viruses by MALDI-TOF mass spectrometry. Intervirology 53:344–353. doi:10.1159/000312919

    Article  PubMed  Google Scholar 

  7. Yoosuf N, Yutin N, Colson P, Shabalina SA, Pagnier I, Robert C, Azza S, Klose T, Wong J, Rossmann MG, La SB, Raoult D, Koonin EV (2012) Related giant viruses in distant locations and different habitats: Acanthamoeba polyphaga moumouvirus represents a third lineage of the Mimiviridae that is close to the megavirus lineage. Genome Biol Evol 4:1324–1330. doi:10.1093/gbe/evs109

    Article  PubMed  CAS  Google Scholar 

  8. Boyer M, Yutin N, Pagnier I, Barrassi L, Fournous G, Espinosa L, Robert C, Azza S, Sun S, Rossmann MG, Suzan-Monti M, La SB, Koonin EV, Raoult D (2009) Giant Marseillevirus highlights the role of amoebae as a melting pot in emergence of chimeric microorganisms. Proc Natl Acad Sci USA 106:21848–21853. doi:10.1073/pnas.0911354106

    Article  PubMed  CAS  Google Scholar 

  9. Thomas V, Bertelli C, Collyn F, Casson N, Telenti A, Goesmann A, Croxatto A, Greub G (2011) Lausannevirus, a giant amoebal virus encoding histone doublets. Environ Microbiol 13:1454–1466. doi:10.1111/j.1462-2920.2011.02446.x

    Article  PubMed  CAS  Google Scholar 

  10. Colson P, Pagnier I, Yoosuf N, Fournous G, La Scola B, Raoult D (2012) Marseilleviridae, a new family of giant viruses infecting amoebae. Arch Virol 158(4):915–920. doi:10.1007/s00705-012-1537-y

    Google Scholar 

  11. Claverie JM, Ogata H, Audic S, Abergel C, Suhre K, Fournier PE (2006) Mimivirus and the emerging concept of “giant” virus. Virus Res 117:133–144. doi:10.1016/j.virusres.2006.01.008

    Article  PubMed  CAS  Google Scholar 

  12. Arslan D, Legendre M, Seltzer V, Abergel C, Claverie JM (2011) Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci USA 108:17486–17491

    Article  PubMed  CAS  Google Scholar 

  13. Fischer MG, Allen MJ, Wilson WH, Suttle CA (2010) Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci USA 107:19508–19513. doi:10.1073/pnas.1007615107

    Article  PubMed  CAS  Google Scholar 

  14. Monier A, Claverie JM, Ogata H (2008) Taxonomic distribution of large DNA viruses in the sea. Genome Biol 9:R106. doi:10.1186/gb-2008-9-7-r106

    Article  PubMed  Google Scholar 

  15. Monier A, Larsen JB, Sandaa RA, Bratbak G, Claverie JM, Ogata H (2008) Marine mimivirus relatives are probably large algal viruses. Virol J 5:12. doi:10.1186/1743-422X-5-12

    Article  PubMed  Google Scholar 

  16. Yamada T (2011) Giant viruses in the environment: their origins and evolution. Curr Opin Virol 1:58–62

    Article  PubMed  Google Scholar 

  17. Kristensen DM, Mushegian AR, Dolja VV, Koonin EV (2010) New dimensions of the virus world discovered through metagenomics. Trends Microbiol 18:11–19. doi:10.1016/j.tim.2009.11.003

    Article  PubMed  CAS  Google Scholar 

  18. Colson P, de Lamballerie X, Fournous G, Raoult D (2012) Reclassification of giant viruses composing a fourth domain of life in the new order Megavirales. Intervirology 55(5):321–332. doi:10.1159/000336562

    Google Scholar 

  19. Yutin N, Koonin EV (2012) Hidden evolutionary complexity of nucleo-cytoplasmic large DNA viruses of eukaryotes. Virol J 9:161

    Article  PubMed  CAS  Google Scholar 

  20. Koonin EV, Yutin N (2010) Origin and evolution of eukaryotic large nucleo-cytoplasmic DNA viruses. Intervirology 53:284–292. doi:10.1159/000312913

    Article  PubMed  Google Scholar 

  21. Krupovic M, Bamford DH (2008) Virus evolution: how far does the double beta-barrel viral lineage extend? Nat Rev Microbiol 6:941–948

    Article  PubMed  CAS  Google Scholar 

  22. Bahar MW, Graham SC, Stuart DI, Grimes JM (2011) Insights into the evolution of a complex virus from the crystal structure of vaccinia virus D13. Structure 19:1011–1020

    Article  PubMed  CAS  Google Scholar 

  23. Bigot Y, Asgari S, Bideshi D, Cheng XW, Federici BA et al. (2011) Family Ascoviridae. In: CM Fauquet, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Virus taxonomy. Ninth report of the international committee on taxonomy of viruses, San Diego, pp 147–152

  24. Szajner P, Weisberg AS, Lebowitz J, Heuser J, Moss B (2005) External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J Cell Biol 170:971–981

    Article  PubMed  CAS  Google Scholar 

  25. Seet BT, Johnston JB, Brunetti CR, Barrett JW, Everett H, Cameron C, Sypula J, Nazarian SH, Lucas A, McFadden G (2003) Poxviruses and immune evasion. Annu Rev Immunol 21:377–423

    Article  PubMed  CAS  Google Scholar 

  26. Werden SJ, Rahman MM, McFadden G (2008) Poxvirus host range genes. Adv Virus Res 71:135–171. doi:10.1016/S0065-3527(08)00003-1

    Article  PubMed  CAS  Google Scholar 

  27. Dixon LK, Abrams CC, Bowick G, Goatley LC, Kay-Jackson PC, Chapman D, Liverani E, Nix R, Silk R, Zhang F (2004) African swine fever virus proteins involved in evading host defence systems. Vet Immunol Immunopathol 100:117–134. doi:10.1016/j.vetimm.2004.04.002

    Article  PubMed  CAS  Google Scholar 

  28. Condit RC (2007) Vaccinia, Inc.—probing the functional substructure of poxviral replication factories. Cell Host Microbe 2:205–207

    Article  PubMed  CAS  Google Scholar 

  29. Mutsafi Y, Zauberman N, Sabanay I, Minsky A (2010) Vaccinia-like cytoplasmic replication of the giant Mimivirus. Proc Natl Acad Sci USA 107:5978–5982. doi:10.1073/pnas.0912737107

    Article  PubMed  CAS  Google Scholar 

  30. Netherton CL, Wileman TE (2013) African swine fever virus organelle rearrangements. Virus Res 173(1):76–86. doi:10.1016/j.virusres.2012.12.014

    Google Scholar 

  31. Novoa RR, Calderita G, Arranz R, Fontana J, Granzow H, Risco C (2005) Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol Cell 97:147–172. doi:10.1042/BC20040058

    Article  PubMed  CAS  Google Scholar 

  32. Netherton CL, Wileman T (2011) Virus factories, double membrane vesicles and viroplasm generated in animal cells. Curr Opin Virol 1:381–387

    Article  PubMed  CAS  Google Scholar 

  33. Keeling PJ (2007) Genomics. Deep questions in the tree of life. Science 317:1875–1876

    Article  PubMed  CAS  Google Scholar 

  34. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ, Gray MW (2005) The tree of eukaryotes. Trends Ecol Evol 20:670–676

    Article  PubMed  Google Scholar 

  35. Koonin EV (2010) The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol 11:209–211

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Natalya Yutin and Eugene V. Koonin are supported by intramural funds of the US Department of Health and Human Services (to the National Library of Medicine). James Van Etten is partially supported by NIH Grant P20 RR15635 from the COBRE Program of the National Center for Research Resources.

Conflict of interest

There are no potential conflicts of interest or financial disclosures for any of the authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Didier Raoult.

Additional information

S. Asgari, Y. Bigot, D. K. Bideshi, X.-W. Cheng and B. A. Federici belong to the Ascoviridae study group of the International Committee on Taxonomy of Viruses (ICTV).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Colson, P., De Lamballerie, X., Yutin, N. et al. “Megavirales”, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch Virol 158, 2517–2521 (2013). https://doi.org/10.1007/s00705-013-1768-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-013-1768-6

Keywords

Navigation