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      Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere

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          Abstract

          Here we report the discovery of two Tupanvirus strains, the longest tailed Mimiviridae members isolated in amoebae. Their genomes are 1.44–1.51 Mb linear double-strand DNA coding for 1276–1425 predicted proteins. Tupanviruses share the same ancestors with mimivirus lineages and these giant viruses present the largest translational apparatus within the known virosphere, with up to 70 tRNA, 20 aaRS, 11 factors for all translation steps, and factors related to tRNA/mRNA maturation and ribosome protein modification. Moreover, two sequences with significant similarity to intronic regions of 18 S rRNA genes are encoded by the tupanviruses and highly expressed. In this translation-associated gene set, only the ribosome is lacking. At high multiplicity of infections, tupanvirus is also cytotoxic and causes a severe shutdown of ribosomal RNA and a progressive degradation of the nucleus in host and non-host cells. The analysis of tupanviruses constitutes a new step toward understanding the evolution of giant viruses.

          Abstract

          Giant viruses are the largest viruses of the known virosphere and their genetic analysis can provide insights into virus evolution. Here, the authors discover Tupanvirus, a unique giant virus that has an unusually long tail and contains the largest translational apparatus of the known virosphere.

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          Most cited references30

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          The 1.2-megabase genome sequence of Mimivirus.

          We recently reported the discovery and preliminary characterization of Mimivirus, the largest known virus, with a 400-nanometer particle size comparable to mycoplasma. Mimivirus is a double-stranded DNA virus growing in amoebae. We now present its 1,181,404-base pair genome sequence, consisting of 1262 putative open reading frames, 10% of which exhibit a similarity to proteins of known functions. In addition to exceptional genome size, Mimivirus exhibits many features that distinguish it from other nucleocytoplasmic large DNA viruses. The most unexpected is the presence of numerous genes encoding central protein-translation components, including four amino-acyl transfer RNA synthetases, peptide release factor 1, translation elongation factor EF-TU, and translation initiation factor 1. The genome also exhibits six tRNAs. Other notable features include the presence of both type I and type II topoisomerases, components of all DNA repair pathways, many polysaccharide synthesis enzymes, and one intein-containing gene. The size and complexity of the Mimivirus genome challenge the established frontier between viruses and parasitic cellular organisms. This new sequence data might help shed a new light on the origin of DNA viruses and their role in the early evolution of eukaryotes.
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            A giant virus in amoebae.

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              Pandoraviruses: amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes.

              Ten years ago, the discovery of Mimivirus, a virus infecting Acanthamoeba, initiated a reappraisal of the upper limits of the viral world, both in terms of particle size (>0.7 micrometers) and genome complexity (>1000 genes), dimensions typical of parasitic bacteria. The diversity of these giant viruses (the Megaviridae) was assessed by sampling a variety of aquatic environments and their associated sediments worldwide. We report the isolation of two giant viruses, one off the coast of central Chile, the other from a freshwater pond near Melbourne (Australia), without morphological or genomic resemblance to any previously defined virus families. Their micrometer-sized ovoid particles contain DNA genomes of at least 2.5 and 1.9 megabases, respectively. These viruses are the first members of the proposed "Pandoravirus" genus, a term reflecting their lack of similarity with previously described microorganisms and the surprises expected from their future study.
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                Author and article information

                Contributors
                didier.raoult@gmail.com
                bernard.la-scola@univ-amu.fr
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                27 February 2018
                27 February 2018
                2018
                : 9
                : 749
                Affiliations
                [1 ]ISNI 0000 0004 0519 5986, GRID grid.483853.1, MEPHI, APHM, IRD 198, Aix Marseille Univ, , IHU-Méditerranee Infection, ; 19-21 Bd Jean Moulin, 13005 Marseille, France
                [2 ]ISNI 0000 0001 2181 4888, GRID grid.8430.f, Laboratório de Vírus, Instituto de Ciências Biológicas, Departamento de Microbiologia, , Universidade Federal de Minas Gerais, ; Belo Horizonte, 31270-901 Brazil
                [3 ]ISNI 0000 0001 2112 9282, GRID grid.4444.0, CNRS, ; 13005 Marseille, France
                [4 ]ISNI 0000 0001 2238 5157, GRID grid.7632.0, Laboratório de Microscopia Eletrônica e Virologia, Departamento de Biologia Celular, Instituto de Ciências Biológicas, , Universidade de Brasília, Asa Norte, ; Brasília, 70910-900 Brazil
                [5 ]ISNI 0000 0001 0144 2976, GRID grid.420953.9, Lab. Biomass Conversion, , Embrapa Pantanal, ; R. 21 de Setembro 1880, 79320-900 Corumbá/MS, Brazil
                [6 ]ISNI 0000 0001 2284 9388, GRID grid.14925.3b, Cell Biology and Metabolomics Platforms, , Gustave Roussy Cancer Campus, ; Villejuif, 94805 France
                [7 ]GRID grid.417925.c, Equipe 11 labellisée Ligue Nationale contre le Cancer, , Centre de Recherche des Cordeliers, ; Paris, 75006 France
                [8 ]ISNI 0000000121866389, GRID grid.7429.8, Institut National de la Santé et de la Recherche Médicale (INSERM), ; Paris, 75654 France
                [9 ]ISNI 0000 0004 1788 6194, GRID grid.469994.f, Université Paris Descartes, , Sorbonne Paris Cité, ; Paris, 75015 France
                [10 ]ISNI 0000 0001 1955 3500, GRID grid.5805.8, Université Pierre et Marie Curie, ; Paris, 75005 France
                [11 ]GRID grid.414093.b, Pôle de Biologie, , Hôpital Européen Georges Pompidou, AP-HP, ; Paris, 75015 France
                [12 ]ISNI 0000 0000 9241 5705, GRID grid.24381.3c, Department of Women’s and Children’s Health, , Karolinska University Hospital, ; Stockholm, SE-171 76 Sweden
                Author information
                http://orcid.org/0000-0002-1061-196X
                http://orcid.org/0000-0002-1076-8617
                Article
                3168
                10.1038/s41467-018-03168-1
                5829246
                29487281
                753e02de-1986-4004-93a8-b31b49470e8d
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 3 October 2017
                : 23 January 2018
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