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Table of Contents
Vol. 53, No. 5, 2010
Issue release date: June 2010
Section title: Paper
Intervirology 2010;53:362–378
(DOI:10.1159/000312921)

Giant Viruses: Conflicts in Revisiting the Virus Concept

Forterre P.a, b
aUnité de Biologie du Gène chez les Extrêmophiles, Institut Pasteur, Paris, and bUnité de Biologie du Gène chez les Extrêmophiles, Institut de Génétique et Microbiologie, Université Paris-Sud CNRS UMR 8621, Orsay, France
email Corresponding Author

Abstract

The current paradigm on the nature of viruses is based on early work of the ‘phage group’ (the pro-phage concept) and molecular biologists working on tumour viruses (the proto-oncogene concept). It posits that viruses evolved from either prokaryotic or eukaryotic cellular genes that became infectious via their association with capsid genes. In this view, after their emergence viruses continued to evolve by stealing cellular genes (the escape model). This paradigm has been challenged recently by scientists who propose that viruses pre-dated modern cells. In particular, the discovery of Mimivirus has stimulated a lot of discussions on the nature of viruses. There are two major schools of thought, those who defend the escape model, suggesting that giant viruses are giant pickpockets (chimera), and those who emphasize their uniqueness and ancient origin. Comparative genomics of Mimivirus and related viruses (nucleo-cytoplasmic large DNA viruses) have produced a lot of data that have been interpreted according to the prejudices of the authors and thus failed until now to generate a consensus. I briefly review here the history of these debates and how they lead to new proposals, such as the definition of viruses as capsid-encoding organisms or else the recognition of their fundamentally cellular nature, the virocell concept.

© 2010 S. Karger AG, Basel


  

Key Words

  • Bacteriophage
  • Horizontal gene transfer
  • Mimivirus
  • Nucleo-cytoplasmic large DNA viruses
  • Tree of life
  • Virocell
  • Virus evolution
  • Virus origin

References

  1. Lwoff A: The concept of virus. J Gen Microbiol 1957;17:239–253.
  2. Lwoff A: Principles of classification and nomenclature of viruses. Nature 1967;215:13–14.
  3. Lwoff A: Interaction among virus, cell, and organism. Science 1966;152:1216–1220.
  4. Temin HM: The DNA provirus hypothesis. Science 1976;192:1075–1080.
  5. Jacob F, Wollman E: Viruses and genes. Sci Am 1961;204:93–107.
  6. Moreira D, López-García P: Comment on ‘The 1.2-megabase genome sequence of Mimivirus’. Science 2005;308:1114.
  7. Moreira D, López-García P: Ten reasons to exclude viruses from the tree of life. Nat Rev Microbiol 2009;7:306–311.
  8. Bandea C: A new theory on the origin and the nature of viruses. J Theor Biol 1983;105:591–602.
  9. Liu LF, Liu CC, Alberts BM: T4 DNA topoisomerase: a new ATP-dependent enzyme essential for initiation of T4 bacteriophage DNA replication. Nature 1979;281:456–461.
  10. Bernad A, Zaballos A, Salas M, Blanco L: Structural and functional relationships between prokaryotic and eukaryotic DNA polymerases. EMBO J 1987;6:4219–4225.
  11. Woese CR, Fox GE: Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 1977;74:5088–5090.
  12. Woese CR: Archaebacteria. Sci Am 1981;244:98.

    External Resources

  13. Forterre P: New hypotheses on the origin of prokaryotes, eukaryotes and viruses; in Trân Thanh Vân JK, Mounolou JC, Schneider J, McKay C (eds): Frontiers of Life. Gif sur Yvette, Editions Frontières, 1991, pp 221–233.
  14. Forterre P: The origin of DNA genomes and DNA replication. Curr Opin Microbiol 2002;5:525–532.
  15. Forterre P: The two ages of the RNA world, and the transition to the DNA world: a story of viruses and cells. Biochimie 2005;87:793–803.
  16. Koonin EV, Senkevich TG, Dolja VV: The ancient virus world and evolution of cells. Biol Direct 2006;9:1–29.

    External Resources

  17. Forterre P: Displacement of cellular proteins by functional analogues from plasmids or viruses could explain puzzling phylogenies of many DNA informational proteins. Mol Microbiol 1999;33:457–465.
  18. Forterre P: The origin of viruses and their possible roles in major evolutionary transitions. Virus Res 2006;117:5–16.
  19. Takemura M: Poxviruses and the origin of the eukaryotic nucleus. J Mol Evol 2001;52:419–425.
  20. Bell PJ: Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus? J Mol Evol 2001;53:251–256.
  21. Forterre P: Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc Natl Acad Sci 2006;103:3669–3674.
  22. Benson SD, Bamford JK, Bamford DH, Burnett RM: Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 1999;98:825–833.
  23. Bamford DH: Do viruses form lineages across different domains of life? Res Microbiol 2003;154:231–236.
  24. Baker ML, Jiang W, Rixon FJ, Chiu W: Common ancestry of herpes viruses and tailed DNA bacteriophages. J Virol2005;79:14967–14970.
  25. Bamford DH, Grimes JM, Stuart DI: What does structure tell us about virus evolution? Curr Opin Struct Biol 2006;15:655–663.

    External Resources

  26. Krupovic M, Bamford DH: Virus evolution: how far does the double beta-barrel viral lineage extend? Nat Rev Microbiol 2008;6:941–948.
  27. Martin A, Yeats S, Janekovic D, Reiter WD, Aicher W, Zillig W: SAV 1, a temperate u.v.-inducible DNA virus-like particle from the archaebacterium Sulfolobus acidocaldarius isolate B12. EMBO J 1984;3:2165–2168.
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  29. La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie JM, Raoult D: A giant virus in amoebae. Science 2003;299:2033.
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  31. Moreira D, Brochier-Armanet C: Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol Biol 2008;8:12.
  32. Claverie JM: Viruses take center stage in cellular evolution. Genome Biol 2006;7:110.
  33. Raoult D, Forterre P: Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol 2008;6:315–319.
  34. Forterre P: Manipulation of cellular syntheses and the nature of viruses: the virocell concept. Comptes Rendus Acad Sci, in press.
  35. Suzan-Monti M, La Scola B, Barrassi L, Espinosa L, Raoult D: Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS ONE 2007;2:e328.
  36. Ogata H, Abergel C, Raoult D, Claverie JM: Response to comment on the 1.2-Megabase genome sequence of Mimivirus. Science 2005;308:1114–1115.
  37. Cavalier-Smith T: Megaphylogeny, cell body plans, adaptive zones: causes and timing of eukaryote basal radiations. J Eukaryot Microbiol 2009;56:26–33.
  38. Claverie JM, Ogata H: Ten good reasons not to exclude giruses from the evolutionary picture. Nat Rev Microbiol 2009;7:615.
  39. López-García P, Moreira D: Yet viruses cannot be included in the tree of life. Nat Rev Microbiol 2009;7:615.

    External Resources

  40. Iyer LM, Balaji S, Koonin EV, Aravind L: Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 2006;117:156–184.
  41. 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.
  42. 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.
  43. Boyer M, Yutin N, Pagnier I, Barrassi L, Fournous G, Espinosa L, Robert C, Azza S, 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 chimeric microorganisms. Proc Natl Acad Sci USA 2009;106:21848–21853.
  44. Dagan T, Martin W: The tree of one percent. Genome Biol 2006;7:118.
  45. Raoult D: There is no such thing as a tree of life (and of course viruses are out!). Nat Rev Microbiol 2009;7:615.
  46. Raoult D: The post-Darwinist rhizome of life. Lancet 2010;375:104–105.
  47. Gribaldo S, Brochier C: Phylogeny of prokaryotes: does it exist and why should we care? Res Microbiol 2009;160:513–521.
  48. Filée 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.
  49. Koonin EV: Virology: Gulliver among the Lilliputians. Curr Biol 2005;15:R167–R169.
  50. Miller ES, Kutter E, Mosig G, Arisaka F, Kunisawa T, Rüger W: Bacteriophage T4 genome. Microbiol Mol Biol Rev 2003;67:86–156.
  51. Filée J, Chandler M: Convergent mechanisms of genome evolution of large giant DNA viruses. Res Microbiol 2008;159:325–331.
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  58. Filée J, Forterre P, Laurent J: The role played by viruses in the evolution of their hosts: a view based on informational protein phylogenies. Res Microbiol 2003;154:237–243.
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  60. 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.
  61. Brochier C, Forterre P, Gribaldo S: An emerging phylogenetic core of Archaea: phylogenies of transcription and translation machineries converge following addition of new genome sequences. BMC Evol Biol 2005;5:36.
  62. Iyer LM, Aravind L, Koonin EV: Common origin of four diverse families of large eukaryotic DNA viruses. J Virol 2001;75:11720–11734.
  63. Koonin EV: Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 2003;1:127–136.
  64. Suhre K: Gene and genome duplication in Acanthamoeba polyphaga Mimivirus. J Virol 2005;79:14095–14101. Erratum in: J Virol 2005;79:15591.
  65. Ogata H, Claverie JM: Unique genes in giant viruses: regular substitution pattern and anomalously short size. Genome Res 2007;17:1353–1361.
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  81. Soler N, Marguet E, Desnoues N, Keller J, Van Tilbeurgh HN, Sezonov G, Forterre P: Two novel families of plasmids from hyperthermophilic archaea encoding new families of replication proteins. Nucleic Acid Res 2010, in press.
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Author Contacts

Patrick Forterre
Unité de Biologie du Gène chez les Extrêmophiles
Institut Pasteur, 25 rue du Docteur Roux
FR–75015 Paris (France)
Tel. +33 1 4568 8791, Fax +33 1 4568 8834, E-Mail forterre@pasteur.fr

  

Article Information

Published online: June 15, 2010
Number of Print Pages : 17
Number of Figures : 9, Number of Tables : 0, Number of References : 82

  

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.

Abstract

The current paradigm on the nature of viruses is based on early work of the ‘phage group’ (the pro-phage concept) and molecular biologists working on tumour viruses (the proto-oncogene concept). It posits that viruses evolved from either prokaryotic or eukaryotic cellular genes that became infectious via their association with capsid genes. In this view, after their emergence viruses continued to evolve by stealing cellular genes (the escape model). This paradigm has been challenged recently by scientists who propose that viruses pre-dated modern cells. In particular, the discovery of Mimivirus has stimulated a lot of discussions on the nature of viruses. There are two major schools of thought, those who defend the escape model, suggesting that giant viruses are giant pickpockets (chimera), and those who emphasize their uniqueness and ancient origin. Comparative genomics of Mimivirus and related viruses (nucleo-cytoplasmic large DNA viruses) have produced a lot of data that have been interpreted according to the prejudices of the authors and thus failed until now to generate a consensus. I briefly review here the history of these debates and how they lead to new proposals, such as the definition of viruses as capsid-encoding organisms or else the recognition of their fundamentally cellular nature, the virocell concept.

© 2010 S. Karger AG, Basel


  

Author Contacts

Patrick Forterre
Unité de Biologie du Gène chez les Extrêmophiles
Institut Pasteur, 25 rue du Docteur Roux
FR–75015 Paris (France)
Tel. +33 1 4568 8791, Fax +33 1 4568 8834, E-Mail forterre@pasteur.fr

  

Article Information

Published online: June 15, 2010
Number of Print Pages : 17
Number of Figures : 9, Number of Tables : 0, Number of References : 82

  

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


Article / Publication Details

First-Page Preview
Abstract of Paper

Published online: 6/15/2010
Issue release date: June 2010

Number of Print Pages: 17
Number of Figures: 9
Number of Tables: 0

ISSN: 0300-5526 (Print)
eISSN: 1423-0100 (Online)

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


Copyright / Drug Dosage

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. Lwoff A: The concept of virus. J Gen Microbiol 1957;17:239–253.
  2. Lwoff A: Principles of classification and nomenclature of viruses. Nature 1967;215:13–14.
  3. Lwoff A: Interaction among virus, cell, and organism. Science 1966;152:1216–1220.
  4. Temin HM: The DNA provirus hypothesis. Science 1976;192:1075–1080.
  5. Jacob F, Wollman E: Viruses and genes. Sci Am 1961;204:93–107.
  6. Moreira D, López-García P: Comment on ‘The 1.2-megabase genome sequence of Mimivirus’. Science 2005;308:1114.
  7. Moreira D, López-García P: Ten reasons to exclude viruses from the tree of life. Nat Rev Microbiol 2009;7:306–311.
  8. Bandea C: A new theory on the origin and the nature of viruses. J Theor Biol 1983;105:591–602.
  9. Liu LF, Liu CC, Alberts BM: T4 DNA topoisomerase: a new ATP-dependent enzyme essential for initiation of T4 bacteriophage DNA replication. Nature 1979;281:456–461.
  10. Bernad A, Zaballos A, Salas M, Blanco L: Structural and functional relationships between prokaryotic and eukaryotic DNA polymerases. EMBO J 1987;6:4219–4225.
  11. Woese CR, Fox GE: Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 1977;74:5088–5090.
  12. Woese CR: Archaebacteria. Sci Am 1981;244:98.

    External Resources

  13. Forterre P: New hypotheses on the origin of prokaryotes, eukaryotes and viruses; in Trân Thanh Vân JK, Mounolou JC, Schneider J, McKay C (eds): Frontiers of Life. Gif sur Yvette, Editions Frontières, 1991, pp 221–233.
  14. Forterre P: The origin of DNA genomes and DNA replication. Curr Opin Microbiol 2002;5:525–532.
  15. Forterre P: The two ages of the RNA world, and the transition to the DNA world: a story of viruses and cells. Biochimie 2005;87:793–803.
  16. Koonin EV, Senkevich TG, Dolja VV: The ancient virus world and evolution of cells. Biol Direct 2006;9:1–29.

    External Resources

  17. Forterre P: Displacement of cellular proteins by functional analogues from plasmids or viruses could explain puzzling phylogenies of many DNA informational proteins. Mol Microbiol 1999;33:457–465.
  18. Forterre P: The origin of viruses and their possible roles in major evolutionary transitions. Virus Res 2006;117:5–16.
  19. Takemura M: Poxviruses and the origin of the eukaryotic nucleus. J Mol Evol 2001;52:419–425.
  20. Bell PJ: Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus? J Mol Evol 2001;53:251–256.
  21. Forterre P: Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc Natl Acad Sci 2006;103:3669–3674.
  22. Benson SD, Bamford JK, Bamford DH, Burnett RM: Viral evolution revealed by bacteriophage PRD1 and human adenovirus coat protein structures. Cell 1999;98:825–833.
  23. Bamford DH: Do viruses form lineages across different domains of life? Res Microbiol 2003;154:231–236.
  24. Baker ML, Jiang W, Rixon FJ, Chiu W: Common ancestry of herpes viruses and tailed DNA bacteriophages. J Virol2005;79:14967–14970.
  25. Bamford DH, Grimes JM, Stuart DI: What does structure tell us about virus evolution? Curr Opin Struct Biol 2006;15:655–663.

    External Resources

  26. Krupovic M, Bamford DH: Virus evolution: how far does the double beta-barrel viral lineage extend? Nat Rev Microbiol 2008;6:941–948.
  27. Martin A, Yeats S, Janekovic D, Reiter WD, Aicher W, Zillig W: SAV 1, a temperate u.v.-inducible DNA virus-like particle from the archaebacterium Sulfolobus acidocaldarius isolate B12. EMBO J 1984;3:2165–2168.
  28. Prangishvili D, Forterre P, Garrett RA: Viruses of the Archaea: a unifying view. Nat Rev Microbiol 2006;4:837–848.
  29. La Scola B, Audic S, Robert C, Jungang L, de Lamballerie X, Drancourt M, Birtles R, Claverie JM, Raoult D: A giant virus in amoebae. Science 2003;299:2033.
  30. 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.
  31. Moreira D, Brochier-Armanet C: Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol Biol 2008;8:12.
  32. Claverie JM: Viruses take center stage in cellular evolution. Genome Biol 2006;7:110.
  33. Raoult D, Forterre P: Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol 2008;6:315–319.
  34. Forterre P: Manipulation of cellular syntheses and the nature of viruses: the virocell concept. Comptes Rendus Acad Sci, in press.
  35. Suzan-Monti M, La Scola B, Barrassi L, Espinosa L, Raoult D: Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS ONE 2007;2:e328.
  36. Ogata H, Abergel C, Raoult D, Claverie JM: Response to comment on the 1.2-Megabase genome sequence of Mimivirus. Science 2005;308:1114–1115.
  37. Cavalier-Smith T: Megaphylogeny, cell body plans, adaptive zones: causes and timing of eukaryote basal radiations. J Eukaryot Microbiol 2009;56:26–33.
  38. Claverie JM, Ogata H: Ten good reasons not to exclude giruses from the evolutionary picture. Nat Rev Microbiol 2009;7:615.
  39. López-García P, Moreira D: Yet viruses cannot be included in the tree of life. Nat Rev Microbiol 2009;7:615.

    External Resources

  40. Iyer LM, Balaji S, Koonin EV, Aravind L: Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 2006;117:156–184.
  41. 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.
  42. 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.
  43. Boyer M, Yutin N, Pagnier I, Barrassi L, Fournous G, Espinosa L, Robert C, Azza S, 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 chimeric microorganisms. Proc Natl Acad Sci USA 2009;106:21848–21853.
  44. Dagan T, Martin W: The tree of one percent. Genome Biol 2006;7:118.
  45. Raoult D: There is no such thing as a tree of life (and of course viruses are out!). Nat Rev Microbiol 2009;7:615.
  46. Raoult D: The post-Darwinist rhizome of life. Lancet 2010;375:104–105.
  47. Gribaldo S, Brochier C: Phylogeny of prokaryotes: does it exist and why should we care? Res Microbiol 2009;160:513–521.
  48. Filée 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.
  49. Koonin EV: Virology: Gulliver among the Lilliputians. Curr Biol 2005;15:R167–R169.
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