Evolutionary genomics of Nucleo-Cytoplasmic Large DNA Viruses

National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA.
Virus Research (Impact Factor: 2.32). 05/2006; 117(1):156-84. DOI: 10.1016/j.virusres.2006.01.009
Source: PubMed


A previous comparative-genomic study of large nuclear and cytoplasmic DNA viruses (NCLDVs) of eukaryotes revealed the monophyletic origin of four viral families: poxviruses, asfarviruses, iridoviruses, and phycodnaviruses [Iyer, L.M., Aravind, L., Koonin, E.V., 2001. Common origin of four diverse families of large eukaryotic DNA viruses. J. Virol. 75 (23), 11720-11734]. Here we update this analysis by including the recently sequenced giant genome of the mimiviruses and several additional genomes of iridoviruses, phycodnaviruses, and poxviruses. The parsimonious reconstruction of the gene complement of the ancestral NCLDV shows that it was a complex virus with at least 41 genes that encoded the replication machinery, up to four RNA polymerase subunits, at least three transcription factors, capping and polyadenylation enzymes, the DNA packaging apparatus, and structural components of an icosahedral capsid and the viral membrane. The phylogeny of the NCLDVs is reconstructed by cladistic analysis of the viral gene complements, and it is shown that the two principal lineages of NCLDVs are comprised of poxviruses grouped with asfarviruses and iridoviruses grouped with phycodnaviruses-mimiviruses. The phycodna-mimivirus grouping was strongly supported by several derived shared characters, which seemed to rule out the previously suggested basal position of the mimivirus [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 (5700), 1344-1350]. These results indicate that the divergence of the major NCLDV families occurred at an early stage of evolution, prior to the divergence of the major eukaryotic lineages. It is shown that subsequent evolution of the NCLDV genomes involved lineage-specific expansion of paralogous gene families and acquisition of numerous genes via horizontal gene transfer from the eukaryotic hosts, other viruses, and bacteria (primarily, endosymbionts and parasites). Amongst the expansions, there are multiple families of predicted virus-specific signaling and regulatory domains. Most NCLDVs have also acquired large arrays of genes related to ubiquitin signaling, and the animal viruses in particular have independently evolved several defenses against apoptosis and immune response, including growth factors and potential inhibitors of cytokine signaling. The mimivirus displays an enormous array of genes of bacterial provenance, including a representative of a new class of predicted papain-like peptidases. It is further demonstrated that a significant number of genes found in NCLDVs also have homologs in bacteriophages, although a vertical relationship between the NCLDVs and a particular bacteriophage group could not be established. On the basis of these observations, two alternative scenarios for the origin of the NCLDVs and other groups of large DNA viruses of eukaryotes are considered. One of these scenarios posits an early assembly of an already large DNA virus precursor from which various large DNA viruses diverged through an ongoing process of displacement of the original genes by xenologous or non-orthologous genes from various sources. The second scenario posits convergent emergence, on multiple occasions, of large DNA viruses from small plasmid-like precursors through independent accretion of similar sets of genes due to strong selective pressures imposed by their life cycles and hosts.

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    • "O VPSA contém um genoma DNA de dupla-fita, linear, complexo e de replicação citoplasmática (Yanez et al. 1995). O virion apresenta um capsídeo icosaédrico regular envolto por um envelope lipoprotéico, de onde emerge a única glicoproteína viral que está associada ao fenômeno de hemadsorção viral (Iyer et al. 2006). O comprimento da molécula de DNA do VPSA varia de 170 to 190kb dependendo do isolado (Nix et al 2006, Villiers et al. 2010). "
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    ABSTRACT: Rev. Bras. Med. Vet., 37(3):255-263, jul/set 2015 255 RESUMO. As técnicas de hemadsorção (HAD) para o isolamento do vírus da Peste Suína Africa-na (PSA) e a fluorescência em amostras de tecido de suínos (FATS) para detecção de antígenos virais foram implantadas na campanha de erradicação da PSA no país. A aplicação das duas técnicas foi ava-Comparação dos métodos virológicos aplicados no diagnóstico da peste suína africana no Brasil, 1978* ABSTRACT. Freitas T.R.P., Souza A.C., Esteves E.G. & Lyra T.M.P. [Compari-son of virological methods applied on african swine fever diagnosis in Bra-zil, 1978.] Comparação dos métodos virológicos aplicados no diagnóstico da peste suína africana no Brasil, 1978. Revista Brasileira de Medicina Veterinária, 37(3):255-263, 2015. Laboratório Nacional Agropecuário, Ministério da Agri-cultura, Pecuária e Abastecimento, Avenida Rômulo Joviano, s/n, Caixa postal 35/50, Pedro Leopoldo, MG 33600-000, Brasil. The techniques of leucocytes haemadsorption (HAD) for the African Swine Fever (ASF) virus isolation and the fluorescent antigens tissue samples (FATS) for virus antigens detection were implanted in the ASF eradication campaign in the country. The complementary of techniques was studied considering the results obtained when the HAD and FATS were concomitantly applied on the same pig tissue samples. The results of 22, 56 and 30 pigs samples from of the States of Rio de Janeiro (RJ), São Paulo (SP) and Paraná (PR), respectively, showed that in RJ 11 (50%); in SP, 28 (50%) and in PR, 15 (50%) samples were positive in the HAD, while, RJ, 18 (82%); SP, 33 (58%) and PR, 17 (57%) were positive in the FATS. In the universe of 108 samples submitted to both the tests, 83 (76.85%) were positive in at least one of the tests, which characterized ASF positivity. Among the positive samples, 28 (34%) have presented HAD negative results and 15 (18%) have presented FATS negative results. The achievement of applying simultaneously the both tests was the reduction of false-negative results, conferring more ASF accurate laboratorial diagnosis, besides to show the tests complementary. This aspect is fundamentally importance concern with a disease eradiation program to must avoid false negative results. Evidences of low virulence ASFV strains in Brazilian ASF outbreaks and also the distribution of ASF outbreaks by the mesoregions of each State were discussed. Public political action to avoid ASFV re-introduction should be thought and established. The successful experience of 1978 can be taken advantage for the country and for the outside.
    Revista brasileira de medicina veterinaria 09/2015; 37(3):155-263. · 0.03 Impact Factor
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    • "This is consistent with the observation that many of the genes in the NCLDVs have been acquired by LGT and are of bacterial origin (Filee and Chandler 2010). Thus, the large value of P of the NCLDVs is not an ancestral state, but derived by the accumulation of extraneous genetic material (Iyer et al. 2006). Several lineages have increased in size independently within the NCLDVs (see Supplementary Figure 1 online). "
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    ABSTRACT: The concept of a "proteomic constraint" proposes that DNA repair capacity is positively correlated with the information content of a genome, which can be approximated to the size of the proteome (P). This in turn implies that DNA repair genes are more likely to be present in genomes with larger values of P. This stands in contrast to the common assumption that informational genes have a core function and so are evenly distributed across organisms. We examined the presence/absence of 18 DNA repair genes in bacterial genomes. A positive relationship between gene presence and P was observed for 17 genes in the total dataset, and 16 genes when only nonintracellular bacteria were examined. A marked reduction of DNA repair genes was observed in intracellular bacteria, consistent with their reduced value of P. We also examined archaeal and DNA virus genomes, and show that the presence of DNA repair genes is likewise related to a larger value of P. In addition, the products of the bacterial genes mutY, vsr, and ndk, involved in the correction of GC/AT mutations, are strongly associated with reduced genome GC content. We therefore propose that a reduction in information content leads to a loss of DNA repair genes and indirectly to a reduction in genome GC content in bacteria by exposure to the underlying AT mutation bias. The reduction in P may also indirectly lead to the increase in substitution rates observed in intracellular bacteria via loss of DNA repair genes. © The American Genetic Association 2015. All rights reserved. For permissions, please e-mail:
    Journal of Heredity 08/2015; DOI:10.1093/jhered/esv055 · 2.09 Impact Factor
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    • "Nucleocytoplasmic large DNA viruses (NCLDVs), or members of the proposed order Megavirales, are the largest known viruses thus far; their genome ranges in size from ≈100 to 2500 kilobase pairs (kbp) and they are visible on photonic microscopy (Iyer et al., 2006; Raoult and Forterre, 2008; Yutin et al., 2009; Yutin and Koonin, 2012; Colson et al., 2013; Philippe et al., 2013; Legendre et al., 2014; Raoult, 2014). These viruses rely on very diverse eukaryotic hosts for their life cycle, which include protists, algae, vertebrate animals, and insects. "
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    ABSTRACT: Nucleocytoplasmic large DNA viruses, or representatives of the proposed order Megavirales, include giant viruses of Acanthamoeba that were discovered over the last 12 years and are bona fide microbes. Phylogenies based on a few genes conserved amongst these megaviruses and shared by microbes classified as Eukarya, Bacteria, and Archaea, allowed for delineation of a fourth monophylogenetic group or "TRUC" (Things Resisting Uncompleted Classification) composed of the Megavirales representatives. A new Megavirales member named Pithovirus sibericum was isolated from a >30,000-year-old dated Siberian permafrost sample. This virion is as large as recently described pandoraviruses but has a genome that is approximately three to four times shorter. Our objective was to update the classification of P. sibericum as a new member of the "Fourth TRUC" club. Phylogenetic trees were constructed based on four conserved ancient genes and a phyletic analysis was concurrently conducted based on the presence/absence patterns of a set of informational genes from members of Megavirales, Bacteria, Archaea, and Eukarya. Phylogenetic analyses based on the four conserved genes revealed that P. sibericum is part of the fourth TRUC composed of Megavirales members, and is closely related to the families Marseilleviridae and Ascoviridae/Iridoviridae. Additionally, hierarchical clustering delineated four branches, and showed that P. sibericum is part of this fourth TRUC. Overall, phylogenetic and phyletic analyses using informational genes clearly indicate that P. sibericum is a new bona fide member of the "Fourth TRUC" club composed of representatives of Megavirales, alongside Bacteria, Archaea, and Eukarya.
    Frontiers in Microbiology 08/2015; 6:722. DOI:10.3389/fmicb.2015.00722 · 3.99 Impact Factor
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