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Archives of Virology

, Volume 158, Issue 12, pp 2517–2521 | Cite as

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

  • Philippe Colson
  • Xavier De Lamballerie
  • Natalya Yutin
  • Sassan Asgari
  • Yves Bigot
  • Dennis K. Bideshi
  • Xiao-Wen Cheng
  • Brian A. Federici
  • James L. Van Etten
  • Eugene V. Koonin
  • Bernard La Scola
  • Didier RaoultEmail author
Original Article

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.

Keywords

Major Capsid Protein Giant Virus Virion Morphogenesis Ancestral Virus Jelly Roll 
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.

Notes

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.

References

  1. 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 PubMedCrossRefGoogle Scholar
  2. 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 PubMedCrossRefGoogle Scholar
  3. 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 PubMedCrossRefGoogle Scholar
  4. 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 PubMedCrossRefGoogle Scholar
  5. 5.
    Claverie JM, Abergel C, Ogata H (2009) Mimivirus. Curr Top Microbiol Immunol 328:89–121PubMedCrossRefGoogle Scholar
  6. 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 PubMedCrossRefGoogle Scholar
  7. 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 PubMedCrossRefGoogle Scholar
  8. 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 PubMedCrossRefGoogle Scholar
  9. 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 PubMedCrossRefGoogle Scholar
  10. 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. 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 PubMedCrossRefGoogle Scholar
  12. 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 108:17486–17491PubMedCrossRefGoogle Scholar
  13. 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 PubMedCrossRefGoogle Scholar
  14. 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 PubMedCrossRefGoogle Scholar
  15. 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 PubMedCrossRefGoogle Scholar
  16. 16.
    Yamada T (2011) Giant viruses in the environment: their origins and evolution. Curr Opin Virol 1:58–62PubMedCrossRefGoogle Scholar
  17. 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 PubMedCrossRefGoogle Scholar
  18. 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. 19.
    Yutin N, Koonin EV (2012) Hidden evolutionary complexity of nucleo-cytoplasmic large DNA viruses of eukaryotes. Virol J 9:161PubMedCrossRefGoogle Scholar
  20. 20.
    Koonin EV, Yutin N (2010) Origin and evolution of eukaryotic large nucleo-cytoplasmic DNA viruses. Intervirology 53:284–292. doi: 10.1159/000312913 PubMedCrossRefGoogle Scholar
  21. 21.
    Krupovic M, Bamford DH (2008) Virus evolution: how far does the double beta-barrel viral lineage extend? Nat Rev Microbiol 6:941–948PubMedCrossRefGoogle Scholar
  22. 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 19:1011–1020PubMedCrossRefGoogle Scholar
  23. 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 147–152Google Scholar
  24. 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 170:971–981PubMedCrossRefGoogle Scholar
  25. 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 21:377–423PubMedCrossRefGoogle Scholar
  26. 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 PubMedCrossRefGoogle Scholar
  27. 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 PubMedCrossRefGoogle Scholar
  28. 28.
    Condit RC (2007) Vaccinia, Inc.—probing the functional substructure of poxviral replication factories. Cell Host Microbe 2:205–207PubMedCrossRefGoogle Scholar
  29. 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 PubMedCrossRefGoogle Scholar
  30. 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. 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 PubMedCrossRefGoogle Scholar
  32. 32.
    Netherton CL, Wileman T (2011) Virus factories, double membrane vesicles and viroplasm generated in animal cells. Curr Opin Virol 1:381–387PubMedCrossRefGoogle Scholar
  33. 33.
    Keeling PJ (2007) Genomics. Deep questions in the tree of life. Science 317:1875–1876PubMedCrossRefGoogle Scholar
  34. 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 20:670–676PubMedCrossRefGoogle Scholar
  35. 35.
    Koonin EV (2010) The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol 11:209–211PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2013

Authors and Affiliations

  • Philippe Colson
    • 1
    • 2
  • Xavier De Lamballerie
    • 2
    • 3
  • Natalya Yutin
    • 4
  • Sassan Asgari
    • 5
  • Yves Bigot
    • 6
  • Dennis K. Bideshi
    • 7
  • Xiao-Wen Cheng
    • 8
  • Brian A. Federici
    • 9
  • James L. Van Etten
    • 10
    • 11
  • Eugene V. Koonin
    • 4
  • Bernard La Scola
    • 1
    • 2
  • Didier Raoult
    • 1
    • 2
    Email author
  1. 1.Unité des Rickettsies, URMITE UMR CNRS 7278 IRD 198 INSERM U1095, Facultés de Médecine et de Pharmacie, IHU Méditerranée InfectionAix-Marseille UniversitéMarseille Cedex 05France
  2. 2.Pôle des Maladies Infectieuses et Tropicales Clinique et Biologique, Fédération de Bactériologie-Hygiène-Virologie, IHU Méditerranée InfectionAssistance Publique, Hôpitaux de Marseille, Centre Hospitalo-Universitaire TimoneMarseille Cedex 05France
  3. 3.Unité des Virus Emergents, UMR190 Emergence des pathologies virales, Faculté de Médecine, Institut de Recherche pour le Développement, EHSP French School of Public HealthAix-Marseille UniversitéMarseilleFrance
  4. 4.National Center for Biotechnology Information (NCBI), National Library of MedicineNational Institutes of HealthBethesdaUSA
  5. 5.School of Biological SciencesThe University of QueenslandSt LuciaAustralia
  6. 6.UMR INRA-CNRS 7247, PRCCentre INRA de NouzillyNouzillyFrance
  7. 7.Molecular and Developmental BiologyUniversity of CaliforniaRiversideUSA
  8. 8.Department of MicrobiologyMiami UniversityOxfordUSA
  9. 9.Department of EntomologyUniversity of CaliforniaRiversideUSA
  10. 10.Department of Plant PathologyUniversity of NebraskaLincolnUSA
  11. 11.Nebraska Center for VirologyUniversity of NebraskaLincolnUSA

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