A Proposed New Order for Eukaryotic Nucleocytoplasmic Large DNA Viruses Philippe Colson Aix-Marseille Universite

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A Proposed New Order for Eukaryotic Nucleocytoplasmic Large DNA Viruses Philippe Colson Aix-Marseille Universite University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Virology Papers Virology, Nebraska Center for 2013 ‘‘Megavirales’’, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses Philippe Colson Aix-Marseille Universite Xavier De Lamballerie EHSP French School of Public Health, Aix-Marseille Universite Natalya Yutin National Institutes of Health Sassan Asgari The University of Queensland Yves Bigot International Committee on Taxonomy of Viruses See next page for additional authors Follow this and additional works at: http://digitalcommons.unl.edu/virologypub Part of the Biological Phenomena, Cell Phenomena, and Immunity Commons, Cell and Developmental Biology Commons, Genetics and Genomics Commons, Infectious Disease Commons, Medical Immunology Commons, Medical Pathology Commons, and the Virology Commons Colson, Philippe; De Lamballerie, Xavier; Yutin, Natalya; Asgari, Sassan; Bigot, Yves; Bideshi, Dennis K.; Cheng, Xiao-Wen; Federici, Brian A.; Van Etten, James L.; Koonin, Eugene V.; La Scola, Bernard; and Raoult, Didier, "‘‘Megavirales’’, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses" (2013). Virology Papers. 268. http://digitalcommons.unl.edu/virologypub/268 This Article is brought to you for free and open access by the Virology, Nebraska Center for at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Virology Papers by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Philippe Colson, Xavier De Lamballerie, Natalya Yutin, Sassan Asgari, Yves Bigot, Dennis K. Bideshi, Xiao- Wen Cheng, Brian A. Federici, James L. Van Etten, Eugene V. Koonin, Bernard La Scola, and Didier Raoult This article is available at DigitalCommons@University of Nebraska - Lincoln: http://digitalcommons.unl.edu/virologypub/268 Arch Virol (2013) 158:2517–2521 DOI 10.1007/s00705-013-1768-6 ORIGINAL ARTICLE ‘‘Megavirales’’, a proposed new order for eukaryotic nucleocytoplasmic large DNA viruses Philippe Colson • Xavier De Lamballerie • Natalya Yutin • Sassan Asgari • Yves Bigot • Dennis K. Bideshi • Xiao-Wen Cheng • Brian A. Federici • James L. Van Etten • Eugene V. Koonin • Bernard La Scola • Didier Raoult Received: 3 August 2012 / Accepted: 7 May 2013 / Published online: 29 June 2013 Ó Springer-Verlag Wien 2013 Abstract The nucleocytoplasmic large DNA viruses replication and virion formation to the last common (NCLDVs) comprise a monophyletic group of viruses that ancestor of all these viruses. Taken together, these char- infect animals and diverse unicellular eukaryotes. The acteristics lead us to propose assigning an official taxo- NCLDV group includes the families Poxviridae, Asfarvir- nomic rank to the NCLDVs as the order ‘‘Megavirales’’, in idae, Iridoviridae, Ascoviridae, Phycodnaviridae, Mimi- reference to the large size of the virions and genomes of viridae and the proposed family ‘‘Marseilleviridae’’. The these viruses. family Mimiviridae includes the largest known viruses, with genomes in excess of one megabase, whereas the genome size in the other NCLDV families varies from 100 Introduction to 400 kilobase pairs. Most of the NCLDVs replicate in the cytoplasm of infected cells, within so-called virus factories. The nucleocytoplasmic large DNA viruses (NCLDVs) are The NCLDVs share a common ancient origin, as demon- an apparently monophyletic group of viruses infecting strated by evolutionary reconstructions that trace approxi- eukaryotes that was first described in 2001 [1]. The mately 50 genes encoding key proteins involved in viral NCLDVs encompass the families Poxviridae, Asfarviridae, Iridoviridae, Ascoviridae, and Phycodnaviridae [1–3] and two groups of distinct giant viruses that have been isolated S. Asgari, Y. Bigot, D. K. Bideshi, X.-W. Cheng and B. A. Federici from Acanthamoeba, giving rise to the now established belong to the Ascoviridae study group of the International Committee family Mimiviridae [4–7] and the proposed family ‘‘Mar- on Taxonomy of Viruses (ICTV). seilleviridae’’ [8–10] (Table 1). P. Colson Á B. La Scola Á D. Raoult (&) N. Yutin Á E. V. Koonin Unite´ des Rickettsies, URMITE UMR CNRS 7278 IRD 198 National Center for Biotechnology Information (NCBI), INSERM U1095, Faculte´sdeMe´decine et de Pharmacie, IHU National Library of Medicine, National Institutes of Health, Me´diterrane´e Infection, Aix-Marseille Universite´, 27 Boulevard Bldg. 38A, 8600 Rockville Pike, Bethesda, MD 20894, USA Jean Moulin, 13385 Marseille Cedex 05, France e-mail: [email protected] S. Asgari School of Biological Sciences, The University of Queensland, P. Colson Á X. De Lamballerie Á B. La Scola Á D. Raoult St Lucia, QLD 4072, Australia Poˆle des Maladies Infectieuses et Tropicales Clinique et Biologique, Fe´de´ration de Bacte´riologie-Hygie`ne-Virologie, Y. Bigot IHU Me´diterrane´e Infection, Assistance Publique, Hoˆpitaux de UMR INRA-CNRS 7247, PRC, Centre INRA de Nouzilly, Marseille, Centre Hospitalo-Universitaire Timone, 264 Rue 37380 Nouzilly, France Saint-Pierre, 13385 Marseille Cedex 05, France D. K. Bideshi X. De Lamballerie Molecular and Developmental Biology, University of California, Unite´ des Virus Emergents, UMR190 Emergence des Riverside, CA 92521, USA pathologies virales, Faculte´ de Me´decine, Institut de Recherche pour le De´veloppement, EHSP French School of Public Health, Aix-Marseille Universite´, Marseille, France 123 2518 P. Colson et al. The viruses of the family Mimiviridae possess by far the the entire group [3]. The maximum-likelihood evolutionary largest virions and genomes among all currently known reconstruction that led to this conclusion relied upon a viruses. Strikingly, mimivirus genomes are larger than phylogenetic tree of the universally conserved NCLDV those of many parasitic and symbiotic bacteria and genes and the patterns of presence-absence of other genes approach the size and complexity of the smallest known as derived from the clusters of orthologous genes of the free-living bacteria and archaea. Moreover, mimiviruses NCLDVs (NCVOGs). Although a comprehensive phylo- encode many genes that have not been found in other genetic analysis of the putative ancestral NCLDV genes viruses, in particular multiple components of the translation revealed a complex picture of evolution that involved system such as aminoacyl-tRNA synthetases [4, 11, 12]. A multiple non-orthologous gene displacements, on the distant relative of mimiviruses, Cafeteria roenbergensis whole, the results of this analysis were compatible with the virus (CroV), has been isolated from a marine stramenopile descent of (nearly) all of these genes from an ancestral [13], and numerous homologs of mimivirus genes have virus [19]. Moreover, the inferred ancestral NCLDV genes been detected in metagenomic samples [14–17], indicating encode proteins that perform key functions in virus genome that the actual diversity of the giant viruses remains largely replication and expression as well as virion morphogenesis untapped. These unusual features of the mimiviruses have and structure, suggesting that the putative ancestral virus attracted strong interest of many researchers and revitalized already possessed the main biological features of the extant the study of molecular biology and biochemistry of the NCLDVs. NCLDVs. Importantly, the set of the approximately 50 ancestral A reclassification of the members of the NCLDV fam- genes sharply partitions the NCLDVs from all other groups ilies into a new virus order ‘‘Megavirales’’ has been sug- of viruses, including large DNA viruses infecting eukary- gested recently [18], based upon several defining features. otes, such as nudiviruses, herpesviruses and baculoviruses, In the present proposal, we succinctly summarize these as well as large DNA viruses of bacteria and archaea. unique traits of the NCLDV and make the formal case for Although some of these viruses share with the NCLDVs the distinctness of the NCLDVs from other large DNA one or more of the ‘‘virus hallmark genes’’, such as the viruses. DNA polymerase, the helicase-primase or the packaging ATPase, none come close to possessing the entire set of the ancestral NCLDV genes [20]. The defining features of the NCLDVs The apparent origin of the NCLDVs from a common ancestral virus is buttressed by shared genomic, structural The monophyly of the NCLDVs, i.e., the common origin of and biological features. With the exception of the members all these viruses from the same ancestral virus, was inferred of the virus families Poxviridae and Ascoviridae, all the from the results of phylogenetic and phyletic analyses [1–3, NCLDVs form large, icosahedral capsids (more than 19]. All of the NCLDVs share five core genes, namely 100 nm in diameter) that are comprised of a single, those encoding the major capsid protein (poxvirus D13 homologous double b barrel jelly roll protein [21] and gene), helicase-primase (D5), DNA polymerase elongation encapsidate a single double-stranded DNA molecule subunit family B, DNA-packaging ATPase (A32), and viral ranging in size from 100 kilobase pairs to over one meg- late transcription factor 3 (A2L). Moreover, approximately abase pairs (Table 1). The exceptions to this conserved 50 genes, although missing in some of the NCLDVs, were virion architecture are the poxviruses and the ascoviruses, assigned, with high confidence, to the common ancestor of with their unique brick-shaped virions and allantoid caps- ids, respectively [22, 23]. However, at least in poxviruses, this appears to be a derived
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