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
- Horizontal gene transfer
- Nucleo-cytoplasmic large DNA viruses
- Tree of life
- Virus evolution
- Virus origin
- Lwoff A: The concept of virus. J Gen Microbiol 1957;17:239–253.
- Lwoff A: Principles of classification and nomenclature of viruses. Nature 1967;215:13–14.
- Lwoff A: Interaction among virus, cell, and organism. Science 1966;152:1216–1220.
- Temin HM: The DNA provirus hypothesis. Science 1976;192:1075–1080.
- Jacob F, Wollman E: Viruses and genes. Sci Am 1961;204:93–107.
- Moreira D, López-García P: Comment on ‘The 1.2-megabase genome sequence of Mimivirus’. Science 2005;308:1114.
- Moreira D, López-García P: Ten reasons to exclude viruses from the tree of life. Nat Rev Microbiol 2009;7:306–311.
- Bandea C: A new theory on the origin and the nature of viruses. J Theor Biol 1983;105:591–602.
- 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.
- Bernad A, Zaballos A, Salas M, Blanco L: Structural and functional relationships between prokaryotic and eukaryotic DNA polymerases. EMBO J 1987;6:4219–4225.
- Woese CR, Fox GE: Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 1977;74:5088–5090.
- Woese CR: Archaebacteria. Sci Am 1981;244:98.
- 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.
- Forterre P: The origin of DNA genomes and DNA replication. Curr Opin Microbiol 2002;5:525–532.
- 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.
- Koonin EV, Senkevich TG, Dolja VV: The ancient virus world and evolution of cells. Biol Direct 2006;9:1–29.
- 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.
- Forterre P: The origin of viruses and their possible roles in major evolutionary transitions. Virus Res 2006;117:5–16.
- Takemura M: Poxviruses and the origin of the eukaryotic nucleus. J Mol Evol 2001;52:419–425.
- Bell PJ: Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus? J Mol Evol 2001;53:251–256.
- 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.
- 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.
- Bamford DH: Do viruses form lineages across different domains of life? Res Microbiol 2003;154:231–236.
- Baker ML, Jiang W, Rixon FJ, Chiu W: Common ancestry of herpes viruses and tailed DNA bacteriophages. J Virol2005;79:14967–14970.
- Bamford DH, Grimes JM, Stuart DI: What does structure tell us about virus evolution? Curr Opin Struct Biol 2006;15:655–663.
- Krupovic M, Bamford DH: Virus evolution: how far does the double beta-barrel viral lineage extend? Nat Rev Microbiol 2008;6:941–948.
- 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.
- Prangishvili D, Forterre P, Garrett RA: Viruses of the Archaea: a unifying view. Nat Rev Microbiol 2006;4:837–848.
- 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.
- 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.
- Moreira D, Brochier-Armanet C: Giant viruses, giant chimeras: the multiple evolutionary histories of Mimivirus genes. BMC Evol Biol 2008;8:12.
- Claverie JM: Viruses take center stage in cellular evolution. Genome Biol 2006;7:110.
- Raoult D, Forterre P: Redefining viruses: lessons from Mimivirus. Nat Rev Microbiol 2008;6:315–319.
- Forterre P: Manipulation of cellular syntheses and the nature of viruses: the virocell concept. Comptes Rendus Acad Sci, in press.
- 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.
- 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.
- Cavalier-Smith T: Megaphylogeny, cell body plans, adaptive zones: causes and timing of eukaryote basal radiations. J Eukaryot Microbiol 2009;56:26–33.
- Claverie JM, Ogata H: Ten good reasons not to exclude giruses from the evolutionary picture. Nat Rev Microbiol 2009;7:615.
- López-García P, Moreira D: Yet viruses cannot be included in the tree of life. Nat Rev Microbiol 2009;7:615.
- Iyer LM, Balaji S, Koonin EV, Aravind L: Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 2006;117:156–184.
- 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.
- 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.
- 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.
- Dagan T, Martin W: The tree of one percent. Genome Biol 2006;7:118.
- Raoult D: There is no such thing as a tree of life (and of course viruses are out!). Nat Rev Microbiol 2009;7:615.
- Raoult D: The post-Darwinist rhizome of life. Lancet 2010;375:104–105.
- Gribaldo S, Brochier C: Phylogeny of prokaryotes: does it exist and why should we care? Res Microbiol 2009;160:513–521.
- 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.
- Koonin EV: Virology: Gulliver among the Lilliputians. Curr Biol 2005;15:R167–R169.
- Miller ES, Kutter E, Mosig G, Arisaka F, Kunisawa T, Rüger W: Bacteriophage T4 genome. Microbiol Mol Biol Rev 2003;67:86–156.
- Filée J, Chandler M: Convergent mechanisms of genome evolution of large giant DNA viruses. Res Microbiol 2008;159:325–331.
- Forterre P, Prangishvili D: The great billion-year war between ribosome- and capsid-encoding organisms (cells and viruses) as the major source of evolutionary novelties. Ann NY Acad Sci 2009;1178:65–77.
- Kristensen DM, Mushegian A, Dolja VV, Koonin EV: New dimensions of the virus world discoverde through metagenomics. Trends Microbiol 2010;18:11–19.
- Cortez D, Forterre P, Gribaldo S: A hidden reservoir of integrative elements is the major source of recently acquired foreign genes and ORFans in archaeal and bacterial genomes. Genome Biol 2009;10:R65.
- De Parseval N, Heidmann T: Human endogenous retroviruses: from infectious elements to human genes. Cytogenet Genome Res 2005;110:318–332.
- Filée 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.
- Filée J, Forterre P, Sen-Lin T, Laurent J: Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J Mol Evol 2002;54:763–773.
- 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.
- Forterre P, Gribaldo S, Gadelle D, Serre MC: Origin and evolution of DNA topoisomerases. Biochimie 2007;89:427–446.
- 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.
- 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.
- Iyer LM, Aravind L, Koonin EV: Common origin of four diverse families of large eukaryotic DNA viruses. J Virol 2001;75:11720–11734.
- Koonin EV: Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 2003;1:127–136.
- Suhre K: Gene and genome duplication in Acanthamoeba polyphaga Mimivirus. J Virol 2005;79:14095–14101. Erratum in: J Virol 2005;79:15591.
- Ogata H, Claverie JM: Unique genes in giant viruses: regular substitution pattern and anomalously short size. Genome Res 2007;17:1353–1361.
- Comeau AM, Krisch HM: War is peace: dispatches from the bacterial and phage killing fields. Curr Opin Microbiol 2005;8:488–494.
- Rancurel C, Khosravi M, Dunker AK, Romero PR, Karlin D: Overlapping genes produce proteins with unusual sequence properties and offer insight into de novo protein creation. J Virol 2009;83:10719–10736.
- Sun S, La Scola B, Bowman VD, Ryan CM, Whitelegge JP, Raoult D, Rossmann MG: Structural studies of the Sputnik virophage. J Virol 2010;84:894–897.
- Kurland CG, Collins LJ, Penny D: Genomics and the irreducible nature of eukaryote cells. Science. 2006;312:1011–1014.
- Poole AM, Penny D: Evaluating hypotheses for the origin of eukaryotes. Bioessays 2007;29:74–84.
- Fuerst JA: Intracellular compartmentation in planctomycetes. Annu Rev Microbiol 2005;59:299–328.
- Novoa RR, Calderita G, Arranz R, Fontana J, Granzow H, Risco C: Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol Cell 2005;97:147–172.
- Miller S, Krijnse-Locker J: Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol 2008;6:363–374.
- Simon LD: Infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope: T4 head morphogenesis. Proc Natl Acad Sci USA 1972;69:907.
- Forterre P, Prangishvili D: The origin of viruses. Res Microbiol 2009;160:466–472.
- Forterre P: Definition of life : the virus viewpoint. Orig Life Evol Biosph 2010;40:151–160.
- Bandea C: The origin and evolution of viruses as molecular organisms. Nature Precedings 2009. http://hdl.handle.net/10101/npre.2009.3886.1 (accessed March 26, 2010).
- Filée J, Bapteste E, Susko E, Krisch HM: A selective barrier to horizontal gene transfer in the T4-type bacteriophages that has preserved a core genome with the viral replication and structural genes. Mol Biol Evol 2006;23:1688–1698.
- Forterre P: Evolution, viral; in Schaechter M (ed): Encyclopedia of Microbiology, ed 3. Oxford, Elsevier, 2009, pp 370–389.
- Krupovic M, Ravantti JJ, Bamford DH: Geminiviruses: a tale of a plasmid becoming a virus. BMC Evol Biol 2009;9:112.
- 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.
- Bandea C: A unifying scenario on the origin and evolution of cellular and viral domains. Nature Precedings 2009. http://hdl.handle.net/10101/npre.2009.3888.1 (accessed March 26, 2010).
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Published online: June 15, 2010
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