Journal Mobile Options
Table of Contents
Vol. 53, No. 5, 2010
Issue release date: June 2010
Section title: Paper
Free Access
Intervirology 2010;53:284–292
(DOI:10.1159/000312913)

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

Abstract

Background/Aims: The nucleo-cytoplasmic large DNA viruses (NCLDV) constitute an apparently monophyletic group that consists of 6 families of viruses infecting a broad variety of eukaryotes. A comprehensive genome comparison and maximum-likelihood reconstruction of NCLDV evolution reveal a set of approximately 50 conserved genes that can be tentatively mapped to the genome of the common ancestor of this class of eukaryotic viruses. We address the origins and evolution of NCLDV. Results: Phylogenetic analysis indicates that some of the major clades of NCLDV infect diverse animals and protists, suggestive of early radiation of the NCLDV, possibly concomitant with eukaryogenesis. The core NCLDV genes seem to have originated from different sources including homologous genes of bacteriophages, bacteria and eukaryotes. These observations are compatible with a scenario of the origin of the NCLDV at an early stage of the evolution of eukaryotes through extensive mixing of genes from widely different genomes. Conclusions: The common ancestor of the NCLDV probably evolved from a bacteriophage as a result of recruitment of numerous eukaryotic and some bacterial genes, and concomitant loss of the majority of phage genes except for a small core of genes coding for proteins essential for virus genome replication and virion formation.

© 2010 S. Karger AG, Basel


  

Key Words

  • Bacteriophage
  • Eukaryogenesis
  • Nucleo-cytoplasmic large DNA viruses, evolution
  • Phylogenetic analysis

References

  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.

  

Author Contacts

Eugene V. Koonin
National Center for Biotechnology Information
National Library of Medicine, National Institutes of Health
Bethesda, MD 20894 (USA)
E-Mail koonin@ncbi.nlm.nih.gov

  

Article Information

Published online: June 15, 2010
Number of Print Pages : 9
Number of Figures : 3, Number of Tables : 2, Number of References : 41

  

Publication Details

Intervirology (International Journal of Basic and Medical Virology)

Vol. 53, No. 5, Year 2010 (Cover Date: June 2010)

Journal Editor: Liebert U.G. (Leipzig)
ISSN: 0300-5526 (Print), eISSN: 1423-0100 (Online)

For additional information: http://www.karger.com/INT


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  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.