This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Iyer, L. M.
Right arrow Articles by Koonin, E. V.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Iyer, L. M.
Right arrow Articles by Koonin, E. V.

 Previous Article  |  Next Article 

Journal of Virology, December 2001, p. 11720-11734, Vol. 75, No. 23
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.23.11720-11734.2001

Common Origin of Four Diverse Families of Large Eukaryotic DNA Viruses

Lakshminarayan M. Iyer, L. Aravind, and Eugene V. Koonin*

National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20894

Received 29 May 2001/Accepted 7 August 2001

Comparative analysis of the protein sequences encoded in the genomes of three families of large DNA viruses that replicate, completely or partly, in the cytoplasm of eukaryotic cells (poxviruses, asfarviruses, and iridoviruses) and phycodnaviruses that replicate in the nucleus reveals 9 genes that are shared by all of these viruses and 22 more genes that are present in at least three of the four compared viral families. Although orthologous proteins from different viral families typically show weak sequence similarity, because of which some of them have not been identified previously, at least five of the conserved genes appear to be synapomorphies (shared derived characters) that unite these four viral families, to the exclusion of all other known viruses and cellular life forms. Cladistic analysis with the genes shared by at least two viral families as evolutionary characters supports the monophyly of poxviruses, asfarviruses, iridoviruses, and phycodnaviruses. The results of genome comparison allow a tentative reconstruction of the ancestral viral genome and suggest that the common ancestor of all of these viral families was a nucleocytoplasmic virus with an icosahedral capsid, which encoded complex systems for DNA replication and transcription, a redox protein involved in disulfide bond formation in virion membrane proteins, and probably inhibitors of apoptosis. The conservation of the disulfide-oxidoreductase, a major capsid protein, and two virion membrane proteins indicates that the odd-shaped virions of poxviruses have evolved from the more common icosahedral virion seen in asfarviruses, iridoviruses, and phycodnaviruses.


* Corresponding author. Mailing address: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bldg. 38A, 8600 Rockville Pike, Bethesda, MD 20894. Phone (310) 435-5913. Fax: (310) 435-7794. E-mail: koonin{at}ncbi.nlm.nih.gov.


Journal of Virology, December 2001, p. 11720-11734, Vol. 75, No. 23
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.23.11720-11734.2001



This article has been cited by other articles:

  • Loh, J., Zhao, G., Presti, R. M., Holtz, L. R., Finkbeiner, S. R., Droit, L., Villasana, Z., Todd, C., Pipas, J. M., Calgua, B., Girones, R., Wang, D., Virgin, H. W. (2009). Detection of Novel Sequences Related to African Swine Fever Virus in Human Serum and Sewage. J. Virol. 83: 13019-13025 [Abstract] [Full Text]  
  • Bisht, H., Weisberg, A. S., Szajner, P., Moss, B. (2009). Assembly and Disassembly of the Capsid-Like External Scaffold of Immature Virions during Vaccinia Virus Morphogenesis. J. Virol. 83: 9140-9150 [Abstract] [Full Text]  
  • Jalasvuori, M., Jaatinen, S. T., Laurinavicius, S., Ahola-Iivarinen, E., Kalkkinen, N., Bamford, D. H., Bamford, J. K. H. (2009). The Closest Relatives of Icosahedral Viruses of Thermophilic Bacteria Are among Viruses and Plasmids of the Halophilic Archaea. J. Virol. 83: 9388-9397 [Abstract] [Full Text]  
  • Wu, G. A., Jun, S.-R., Sims, G. E., Kim, S.-H. (2009). Whole-proteome phylogeny of large dsDNA virus families by an alignment-free method. Proc. Natl. Acad. Sci. USA 106: 12826-12831 [Abstract] [Full Text]  
  • Jeudy, S., Lartigue, A., Claverie, J.-M., Abergel, C. (2009). Dissecting the Unique Nucleotide Specificity of Mimivirus Nucleoside Diphosphate Kinase. J. Virol. 83: 7142-7150 [Abstract] [Full Text]  
  • Cherrier, M. V., Kostyuchenko, V. A., Xiao, C., Bowman, V. D., Battisti, A. J., Yan, X., Chipman, P. R., Baker, T. S., Van Etten, J. L., Rossmann, M. G. (2009). An icosahedral algal virus has a complex unique vertex decorated by a spike. Proc. Natl. Acad. Sci. USA 106: 11085-11089 [Abstract] [Full Text]  
  • Liao, Y.-C., Shih, Y.-P., Lo, S. H. (2008). Mutations in the Focal Adhesion Targeting Region of Deleted in Liver Cancer-1 Attenuate Their Expression and Function. Cancer Res. 68: 7718-7722 [Abstract] [Full Text]  
  • Hyun, J.-K., Coulibaly, F., Turner, A. P., Baker, E. N., Mercer, A. A., Mitra, A. K. (2007). The Structure of a Putative Scaffolding Protein of Immature Poxvirus Particles as Determined by Electron Microscopy Suggests Similarity with Capsid Proteins of Large Icosahedral DNA Viruses. J. Virol. 81: 11075-11083 [Abstract] [Full Text]  
  • Ogata, H., Claverie, J.-M. (2007). Unique genes in giant viruses: Regular substitution pattern and anomalously short size. Genome Res 17: 1353-1361 [Abstract] [Full Text]  
  • Wang, Y., Kleespies, R. G., Huger, A. M., Jehle, J. A. (2007). The Genome of Gryllus bimaculatus Nudivirus Indicates an Ancient Diversification of Baculovirus-Related Nonoccluded Nudiviruses of Insects. J. Virol. 81: 5395-5406 [Abstract] [Full Text]  
  • Bidle, K. D., Haramaty, L., Barcelos e Ramos, J., Falkowski, P. (2007). Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc. Natl. Acad. Sci. USA 104: 6049-6054 [Abstract] [Full Text]  
  • Boyle, K. A., Arps, L., Traktman, P. (2007). Biochemical and Genetic Analysis of the Vaccinia Virus D5 Protein: Multimerization-Dependent ATPase Activity Is Required To Support Viral DNA Replication. J. Virol. 81: 844-859 [Abstract] [Full Text]  
  • Liao, Y.-C., Si, L., deVere White, R. W., Lo, S. H. (2007). The phosphotyrosine-independent interaction of DLC-1 and the SH2 domain of cten regulates focal adhesion localization and growth suppression activity of DLC-1. JCB 176: 43-49 [Abstract] [Full Text]  
  • Renesto, P., Abergel, C., Decloquement, P., Moinier, D., Azza, S., Ogata, H., Fourquet, P., Gorvel, J.-P., Claverie, J.-M. (2006). Mimivirus Giant Particles Incorporate a Large Fraction of Anonymous and Unique Gene Products. J. Virol. 80: 11678-11685 [Abstract] [Full Text]  
  • Epifano, C., Krijnse-Locker, J., Salas, M. L., Salas, J., Rodriguez, J. M. (2006). Generation of Filamentous Instead of Icosahedral Particles by Repression of African Swine Fever Virus Structural Protein pB438L. J. Virol. 80: 11456-11466 [Abstract] [Full Text]  
  • Osheroff, N. (2006). Unraveling the Structure of the Variola Topoisomerase IB-DNA Complex: A Possible New Twist on Smallpox Therapy.. Mol. Interv. 6: 245-248 [Abstract] [Full Text]  
  • Allen, M. J., Forster, T., Schroeder, D. C., Hall, M., Roy, D., Ghazal, P., Wilson, W. H. (2006). Locus-specific gene expression pattern suggests a unique propagation strategy for a giant algal virus.. J. Virol. 80: 7699-7705 [Abstract] [Full Text]  
  • Su, H.-P., Lin, D. Y.-w., Garboczi, D. N. (2006). The structure of g4, the poxvirus disulfide oxidoreductase essential for virus maturation and infectivity.. J. Virol. 80: 7706-7713 [Abstract] [Full Text]  
  • Ilouze, M., Dishon, A., Kotler, M. (2006). Characterization of a Novel Virus Causing a Lethal Disease in Carp and Koi. Microbiol. Mol. Biol. Rev. 70: 147-156 [Abstract] [Full Text]  
  • Allen, M. J., Schroeder, D. C., Holden, M. T. G., Wilson, W. H. (2006). Evolutionary History of the Coccolithoviridae. Mol Biol Evol 23: 86-92 [Abstract] [Full Text]  
  • Suhre, K. (2005). Gene and Genome Duplication in Acanthamoeba polyphaga Mimivirus. J. Virol. 79: 14095-14101 [Abstract] [Full Text]  
  • Suhre, K., Audic, S., Claverie, J.-M. (2005). Mimivirus gene promoters exhibit an unprecedented conservation among all eukaryotes. Proc. Natl. Acad. Sci. USA 102: 14689-14693 [Abstract] [Full Text]  
  • Bubeck, J. A., Pfitzner, A. J. P. (2005). Isolation and characterization of a new type of chlorovirus that infects an endosymbiotic Chlorella strain of the heliozoon Acanthocystis turfacea. J. Gen. Virol. 86: 2871-2877 [Abstract] [Full Text]  
  • Szajner, P., Weisberg, A. S., Lebowitz, J., Heuser, J., Moss, B. (2005). External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. JCB 170: 971-981 [Abstract] [Full Text]  
  • Wilson, W. H., Schroeder, D. C., Allen, M. J., Holden, M. T. G., Parkhill, J., Barrell, B. G., Churcher, C., Hamlin, N., Mungall, K., Norbertczak, H., Quail, M. A., Price, C., Rabbinowitsch, E., Walker, D., Craigon, M., Roy, D., Ghazal, P. (2005). Complete Genome Sequence and Lytic Phase Transcription Profile of a Coccolithovirus. Science 309: 1090-1092 [Abstract] [Full Text]  
  • Bamford, D. H., Ravantti, J. J., Ronnholm, G., Laurinavicius, S., Kukkaro, P., Dyall-Smith, M., Somerharju, P., Kalkkinen, N., Bamford, J. K. H. (2005). Constituents of SH1, a Novel Lipid-Containing Virus Infecting the Halophilic Euryarchaeon Haloarcula hispanica. J. Virol. 79: 9097-9107 [Abstract] [Full Text]  
  • Yan, X., Chipman, P. R., Castberg, T., Bratbak, G., Baker, T. S. (2005). The Marine Algal Virus PpV01 Has an Icosahedral Capsid with T=219 Quasisymmetry. J. Virol. 79: 9236-9243 [Abstract] [Full Text]  
  • Iyer, L. M., Koonin, E. V., Leipe, D. D., Aravind, L. (2005). Origin and evolution of the archaeo-eukaryotic primase superfamily and related palm-domain proteins: structural insights and new members. Nucleic Acids Res 33: 3875-3896 [Abstract] [Full Text]  
  • Ogata, H., Abergel, C., Raoult, D., Claverie, J.-M. (2005). Response to Comment on "The 1.2-Megabase Genome Sequence of Mimivirus". Science 308: 1114b-1114b [Full Text]  
  • Heuser, J. (2005). Deep-etch EM reveals that the early poxvirus envelope is a single membrane bilayer stabilized by a geodetic "honeycomb" surface coat. JCB 169: 269-283 [Abstract] [Full Text]  
  • Lucet, I. S., Tynan, F. E., Adams, V., Rossjohn, J., Lyras, D., Rood, J. I. (2005). Identification of the Structural and Functional Domains of the Large Serine Recombinase TnpX from Clostridium perfringens. J. Biol. Chem. 280: 2503-2511 [Abstract] [Full Text]  
  • Raoult, D., Audic, S., Robert, C., Abergel, C., Renesto, P., Ogata, H., La Scola, B., Suzan, M., Claverie, J.-M. (2004). The 1.2-Megabase Genome Sequence of Mimivirus. Science 306: 1344-1350 [Abstract] [Full Text]  
  • Espagne, E., Dupuy, C., Huguet, E., Cattolico, L., Provost, B., Martins, N., Poirie, M., Periquet, G., Drezen, J. M. (2004). Genome Sequence of a Polydnavirus: Insights into Symbiotic Virus Evolution. Science 306: 286-289 [Abstract] [Full Text]  
  • Iyer, L. M., Makarova, K. S., Koonin, E. V., Aravind, L. (2004). 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 32: 5260-5279 [Abstract] [Full Text]  
  • Markine-Goriaynoff, N., Gillet, L., Van Etten, J. L., Korres, H., Verma, N., Vanderplasschen, A. (2004). Glycosyltransferases encoded by viruses. J. Gen. Virol. 85: 2741-2754 [Abstract] [Full Text]  
  • Greub, G., Raoult, D. (2004). Microorganisms Resistant to Free-Living Amoebae. Clin. Microbiol. Rev. 17: 413-433 [Abstract] [Full Text]  
  • Stasiak, K., Renault, S., Demattei, M.-V., Bigot, Y., Federici, B. A. (2003). Evidence for the evolution of ascoviruses from iridoviruses. J. Gen. Virol. 84: 2999-3009 [Abstract] [Full Text]  
  • Bideshi, D. K., Renault, S., Stasiak, K., Federici, B. A., Bigot, Y. (2003). Phylogenetic analysis and possible function of bro-like genes, a multigene family widespread among large double-stranded DNA viruses of invertebrates and bacteria. J. Gen. Virol. 84: 2531-2544 [Abstract] [Full Text]  
  • Hughes, A. L., Friedman, R. (2003). Genome-Wide Survey for Genes Horizontally Transferred from Cellular Organisms to Baculoviruses. Mol Biol Evol 20: 979-987 [Abstract] [Full Text]  
  • Scola, B. L., Audic, S., Robert, C., Jungang, L., de Lamballerie, X., Drancourt, M., Birtles, R., Claverie, J.-M., Raoult, D. (2003). A Giant Virus in Amoebae. Science 299: 2033-2033 [Full Text]  
  • Heath, C. M., Windsor, M., Wileman, T. (2003). Membrane Association Facilitates the Correct Processing of pp220 during Production of the Major Matrix Proteins of African Swine Fever Virus. J. Virol. 77: 1682-1690 [Abstract] [Full Text]  
  • Gong, C., Shuman, S. (2002). Chlorella Virus RNA Triphosphatase. MUTATIONAL ANALYSIS AND MECHANISM OF INHIBITION BY TRIPOLYPHOSPHATE. J. Biol. Chem. 277: 15317-15324 [Abstract] [Full Text]