Skip to main content
SpringerLink
Log in

A Decade of Giant Virus Genomics: Surprising Discoveries Opening New Questions

  • Chapter
Global Virology I - Identifying and Investigating Viral Diseases

Abstract

During the last decade, viral studies have investigated truly large viruses for the first time in the history of biology. Those giants of viruses include Acanthamoeba polyphaga mimivirus with a 1.18 Mbp dsDNA genome encoding more than 1,000 genes and a recently isolated “Pandoravirus salinus” (currently unclassified) with a 2.77 Mbp dsDNA genome encoding 2,556 genes. They are part of the classically defined nucleocytoplasmic large DNA virus group, but they generate large virions that are comparable in size with bacterial cells. The discovery of giant viruses has triggered the reexamination of classical virus perceptions, such as “viruses are non-organisms,” and has elicited provocative proposals related to the nature of viruses. In this chapter, we review the fascinating biology of giant viruses uncovered by genomics during recent years. Then we introduce several proposed hypotheses related to the origin and nature of those giant viruses, including the fourth domain hypothesis, the viral eukaryogenesis hypothesis, and the virocell concept. Giant virus research is still in its infancy, but is likely to reveal increasingly fascinating biological phenomena and is expected to engender a novel evolutionary perspective unifying the viral and cellular worlds.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Lwoff A. The concept of virus: the third Marjory Stephenson memorial lecture. J Gen Microbiol. 1957;17:239–53.

    Article  CAS  PubMed  Google Scholar 

  2. 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;306:1344–50.

    Article  CAS  PubMed  Google Scholar 

  3. Rossmann MG. Structure of viruses: a short history. Q Rev Biophys. 2013;46:133–80.

    Article  CAS  PubMed  Google Scholar 

  4. Claverie JM, Abergel C, Ogata H. Mimivirus. Curr Top Microbiol Immunol. 2009;328:89–121.

    CAS  PubMed  Google Scholar 

  5. Legendre M, Santini S, Rico A, Abergel C, Claverie JM. Breaking the 1000-gene barrier for Mimivirus using ultra-deep genome and transcriptome sequencing. Virol J. 2011;8:99.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Legendre M, Audic S, Poirot O, Hingamp P, Seltzer V, Byrne D, Lartigue A, Lescot M, Bernadac A, Poulain J, Abergel C, Claverie JM. mRNA deep sequencing reveals 75 new genes and a complex transcriptional landscape in Mimivirus. Genome Res. 2010;20:664–74.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. 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. 2009;6:223.

    Article  PubMed Central  PubMed  Google Scholar 

  8. Colson P, De Lamballerie X, Yutin N, Asgari S, Bigot Y, Bideshi DK, Cheng XW, Federici BA, Van Etten JL, Koonin EV, La Scola B, Raoult D. “Megavirales”, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses. Arch Virol. 2013;158:2517–21.

    Article  PubMed Central  PubMed  Google Scholar 

  9. Van Etten JL, Meints RH. Giant viruses infecting algae. Annu Rev Microbiol. 1999;53:447–94.

    Article  PubMed  Google Scholar 

  10. Claverie JM, Ogata H, Audic S, Abergel C, Suhre K, Fournier PE. Mimivirus and the emerging concept of “giant” virus. Virus Res. 2006;117:133–44.

    Article  CAS  PubMed  Google Scholar 

  11. Ghedin E, Claverie JM. Mimivirus relatives in the Sargasso Sea. Virol J. 2005;2:62.

    Article  PubMed Central  PubMed  Google Scholar 

  12. Monier A, Claverie JM, Ogata H. Taxonomic distribution of large DNA viruses in the sea. Genome Biol. 2008;9:R106.

    Article  PubMed Central  PubMed  Google Scholar 

  13. Pagnier I, Reteno DG, Saadi H, Boughalmi M, Gaia M, Slimani M, Ngounga T, Bekliz M, Colson P, Raoult D, La Scola B. A decade of improvements in Mimiviridae and Marseilleviridae isolation from amoeba. Intervirology. 2013;56:354–63.

    Article  PubMed  Google Scholar 

  14. Fischer MG, Allen MJ, Wilson WH, Suttle CA. Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci U S A. 2010;107:19508–13.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Arslan D, Legendre M, Seltzer V, Abergel C, Claverie JM. Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci U S A. 2011;108:17486–91.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Philippe N, Legendre M, Doutre G, Coute Y, Poirot O, Lescot M, Arslan D, Seltzer V, Bertaux L, Bruley C, Garin J, Claverie JM, Abergel C. Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science. 2013;341:281–6.

    Article  CAS  PubMed  Google Scholar 

  17. Yutin N, Koonin EV. Pandoraviruses are highly derived phycodnaviruses. Biol Direct. 2013;8:25.

    Article  PubMed Central  PubMed  Google Scholar 

  18. Zauberman N, Mutsafi Y, Halevy DB, Shimoni E, Klein E, Xiao C, Sun S, Minsky A. Distinct DNA exit and packaging portals in the virus Acanthamoeba polyphaga mimivirus. PLoS Biol. 2008;6:e114.

    Article  PubMed Central  PubMed  Google Scholar 

  19. 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;455:100–4.

    Article  PubMed  Google Scholar 

  20. Yutin N, Raoult D, Koonin EV. Virophages, polintons, and transpovirons: a complex evolutionary network of diverse selfish genetic elements with different reproduction strategies. Virol J. 2013;10:158.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Fischer MG, Suttle CA. A virophage at the origin of large DNA transposons. Science. 2011;332:231–4.

    Article  CAS  PubMed  Google Scholar 

  22. Yau S, Lauro FM, DeMaere MZ, Brown MV, Thomas T, Raftery MJ, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Gibson JA, Cavicchioli R. Virophage control of Antarctic algal host-virus dynamics. Proc Natl Acad Sci U S A. 2011;108:6163–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Santini S, Jeudy S, Bartoli J, Poirot O, Lescot M, Abergel C, Barbe V, Wommack KE, Noordeloos AA, Brussaard CP, Claverie JM. Genome of Phaeocystis globosa virus PgV-16 T highlights the common ancestry of the largest known DNA viruses infecting eukaryotes. Proc Natl Acad Sci U S A. 2013;110:10800–5.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Ogata H, Claverie JM. Microbiology. How to infect a mimivirus. Science. 2008;321:1305–6.

    Article  CAS  PubMed  Google Scholar 

  25. Colson P, Gimenez G, Boyer M, Fournous G, Raoult D. The giant Cafeteria roenbergensis virus that infects a widespread marine phagocytic protist is a new member of the fourth domain of Life. PLoS One. 2011;6:e18935.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Legendre M, Arslan D, Abergel C, Claverie JM. Genomics of Megavirus and the elusive fourth domain of Life. Commun Integr Biol. 2012;5:102–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Nasir A, Kim KM, Caetano-Anolles G. Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya. BMC Evol Biol. 2012;12:156.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Wu D, Wu M, Halpern A, Rusch DB, Yooseph S, Frazier M, Venter JC, Eisen JA. Stalking the fourth domain in metagenomic data: searching for, discovering, and interpreting novel, deep branches in marker gene phylogenetic trees. PLoS One. 2011;6:e18011.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Claverie JM, Ogata H. Ten good reasons not to exclude giruses from the evolutionary picture. Nat Rev Microbiol. 2009;7:615. author reply 615.

    Article  CAS  PubMed  Google Scholar 

  30. Moreira D, Lopez-Garcia P. Comment on “The 1.2-megabase genome sequence of Mimivirus”. Science. 2005;308:1114. author reply 1114.

    Article  CAS  PubMed  Google Scholar 

  31. Moreira D, Lopez-Garcia P. Ten reasons to exclude viruses from the tree of life. Nat Rev Microbiol. 2009;7:306–11.

    CAS  PubMed  Google Scholar 

  32. Williams TA, Embley TM, Heinz E. Informational gene phylogenies do not support a fourth domain of life for nucleocytoplasmic large DNA viruses. PLoS One. 2011;6:e21080.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Moreira D, Brochier-Armanet C. Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol Biol. 2008;8:12.

    Article  PubMed Central  PubMed  Google Scholar 

  34. Monier A, Claverie JM, Ogata H. Horizontal gene transfer and nucleotide compositional anomaly in large DNA viruses. BMC Genomics. 2007;8:456.

    Article  PubMed Central  PubMed  Google Scholar 

  35. Forterre P. Giant viruses: conflicts in revisiting the virus concept. Intervirology. 2010;53:362–78.

    Article  PubMed  Google Scholar 

  36. Ogata H, Claverie JM. Unique genes in giant viruses: regular substitution pattern and anomalously short size. Genome Res. 2007;17:1353–61.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Moreau H, Piganeau G, Desdevises Y, Cooke R, Derelle E, Grimsley N. Marine prasinovirus genomes show low evolutionary divergence and acquisition of protein metabolism genes by horizontal gene transfer. J Virol. 2010;84:12555–63.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Sanjuan R, Nebot MR, Chirico N, Mansky LM, Belshaw R. Viral mutation rates. J Virol. 2010;84:9733–48.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Goldenfeld N, Pace NR. Retrospective. Carl R. Woese (1928-2012). Science. 2013;339:661.

    Article  CAS  PubMed  Google Scholar 

  40. Williams TA, Foster PG, Cox CJ, Embley TM. An archaeal origin of eukaryotes supports only two primary domains of life. Nature. 2013;504:231–6.

    Article  CAS  PubMed  Google Scholar 

  41. Villarreal LP, DeFilippis VR. A hypothesis for DNA viruses as the origin of eukaryotic replication proteins. J Virol. 2000;74:7079–84.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Takemura M. Poxviruses and the origin of the eukaryotic nucleus. J Mol Evol. 2001;52:419–25.

    CAS  PubMed  Google Scholar 

  43. Bell PJ. Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus? J Mol Evol. 2001;53:251–6.

    Article  CAS  PubMed  Google Scholar 

  44. Tolonen N, Doglio L, Schleich S, Krijnse Locker J. Vaccinia virus DNA replication occurs in endoplasmic reticulum-enclosed cytoplasmic mini-nuclei. Mol Biol Cell. 2001;12:2031–46.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Bell PJ. Sex and the eukaryotic cell cycle is consistent with a viral ancestry for the eukaryotic nucleus. J Theor Biol. 2006;243:54–63.

    Article  CAS  PubMed  Google Scholar 

  46. Claverie JM. Viruses take center stage in cellular evolution. Genome Biol. 2006;7:110.

    Article  PubMed Central  PubMed  Google Scholar 

  47. Moreira D, Lopez-Garcia P. Symbiosis between methanogenic archaea and delta-proteobacteria as the origin of eukaryotes: the syntrophic hypothesis. J Mol Evol. 1998;47:517–30.

    Article  CAS  PubMed  Google Scholar 

  48. Cavalier-Smith T. Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution. Biol Direct. 2010;5:7.

    Article  PubMed Central  PubMed  Google Scholar 

  49. Martin W, Koonin EV. Introns and the origin of nucleus-cytosol compartmentalization. Nature. 2006;440:41–5.

    Article  CAS  PubMed  Google Scholar 

  50. Raoult D, Forterre P. Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol. 2008;6:315–9.

    Article  CAS  PubMed  Google Scholar 

  51. Forterre P. The virocell concept and environmental microbiology. ISME J. 2013;7:233–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Dolja VV, Krupovic M. Accelerating expansion of the viral universe. Curr Opin Virol. 2013;3:542–5.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Bioinformatics Center, Institute for Chemical Research, Kyoto University, Uji, Kyoto, 611-0011, Japan

    Hiroyuki Ogata Dr. Sc.

  2. Faculty of Science, Tokyo University of Science, Tokyo, 162-8601, Japan

    Masaharu Takemura Dr. Med. Sc.

Authors
  1. Hiroyuki Ogata Dr. Sc.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masaharu Takemura Dr. Med. Sc.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroyuki Ogata Dr. Sc. .

Editor information

Editors and Affiliations

  1. Division of Infectious Diseases and International Medicine, USF Morsani College of Medicine, Tampa, Florida, USA

    Paul Shapshak

  2. Infectious Diseases and International He, USF Morsani College of Medicine, Tampa, Florida, USA

    John T. Sinnott

  3. Division of Infectious Diseases and Inte, USF Morsani College of Medicine, Tampa, Florida, USA

    Charurut Somboonwit

  4. C.W. Bill Young Center for Biodefense & Emerging Infectious Diseases, NIH-NIAID Div. Clinical Research, Frederick, Maryland, USA

    Jens H. Kuhn

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Ogata, H., Takemura, M. (2015). A Decade of Giant Virus Genomics: Surprising Discoveries Opening New Questions. In: Shapshak, P., Sinnott, J., Somboonwit, C., Kuhn, J. (eds) Global Virology I - Identifying and Investigating Viral Diseases. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2410-3_8

Download citation

Publish with us

Policies and ethics

Search

Navigation