Tailed giant Tupanvirus possesses the most complete translational apparatus of the known virosphere
Jônatas Abrahão, Lorena Silva, Ludmila Santos Silva, Jacques Yaacoub Bou Khalil, Rodrigo Rodrigues, Thalita Arantes, Felipe Assis, Paulo Boratto, Miguel Andrade, Erna Geessien Kroon, Bergmann Ribeiro, Ivan Bergier, Herve Seligmann, Eric Ghigo, Philippe Colson, Anthony Levasseur, Guido Kroemer, Didier Raoult & Bernard La Scola
Nature Communications volume 9, Article number: 749 (2018)
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Evolution Microbial genetics Virology
Received: 03 October 2017 Accepted: 23 January 2018
Published online: 27 February 2018
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.
Acknowledgements
We thank our colleagues from URMITE and Laboratório de Vírus of Universidade Federal de Minas Gerais for their assistance, particularly Julien Andreani, Jean-Pierre Baudoin, Gilles Audoly, Amina Cherif Louazani, Lina Barrassi, Priscilla Jardot, Eric Chabrières, Philippe Decloquement, Nicholas Armstrong, Said Azza, Emeline Baptiste, Claudio Bonjardim, Paulo Ferreira, Giliane Trindade and Betania Drumond. In addition, we thank the Méditerranée Infection Foundation, Centro de Microscopia da UFMG, CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and FAPEMIG (Fundação de Amparo à Pesquisa do estado de Minas Gerais) for their financial support. We thank Petrobras for the collection of sediments from ocean. This work was also supported by the French Government under the « Investissements d’avenir » (Investments for the Future) program managed by the Agence Nationale de la Recherche (ANR, fr: National Agency for Research), (reference: Méditerranée Infection 10-IAHU-03). J.A., B.R. and E.K. are CNPq researchers. B.L.S., J.A., L.S., P.C., and E.G.K. are members of a CAPES-COFECUB project.
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Author notes
Jônatas Abrahão, Lorena Silva and Ludmila Santos Silva contributed equally to this work.
Affiliations
MEPHI, APHM, IRD 198, Aix Marseille Univ, IHU-Méditerranee Infection, 19-21 Bd Jean Moulin, 13005, Marseille, France
Jônatas Abrahão, Lorena Silva, Ludmila Santos Silva, Herve Seligmann, Eric Ghigo, Philippe Colson, Anthony Levasseur, Didier Raoult & Bernard La Scola
Laboratório de Vírus, Instituto de Ciências Biológicas, Departamento de Microbiologia, Universidade Federal de Minas Gerais, Belo Horizonte, 31270-901, Brazil
Jônatas Abrahão, Lorena Silva, Ludmila Santos Silva, Rodrigo Rodrigues, Thalita Arantes, Felipe Assis, Paulo Boratto & Erna Geessien Kroon
CNRS, 13005, Marseille, France
Jacques Yaacoub Bou Khalil
Laboratório de Microscopia Eletrônica e Virologia, Departamento de Biologia Celular, Instituto de Ciências Biológicas, Universidade de Brasília, Asa Norte, Brasília, 70910-900, Brazil
Miguel Andrade & Bergmann Ribeiro
Lab. Biomass Conversion, Embrapa Pantanal, R. 21 de Setembro 1880, 79320-900, Corumbá/MS, Brazil
Ivan Bergier
Cell Biology and Metabolomics Platforms, Gustave Roussy Cancer Campus, Villejuif, 94805, France
Guido Kroemer
Equipe 11 labellisée Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers, Paris, 75006, France
Guido Kroemer
Institut National de la Santé et de la Recherche Médicale (INSERM), Paris, 75654, France
Guido Kroemer
Université Paris Descartes, Sorbonne Paris Cité, Paris, 75015, France
Guido Kroemer
Université Pierre et Marie Curie, Paris, 75005, France
Guido Kroemer
Pôle de Biologie, Hôpital Européen Georges Pompidou, AP-HP, Paris, 75015, France
Guido Kroemer
Department of Women’s and Children’s Health, Karolinska University Hospital, Stockholm, SE-171 76, Sweden
Guido Kroemer
Contributions
D.R., B.L.S., J.S.A., A.L., P.C., E.G.K, and E.G. designed the study and experiments. L.S., J.S.A, J.B.K., R.R., L.S., L.S.S., T.A., P.C., F.A. P.B., M.A., I.B., B.R., A.L., and H.S. performed sample collection, virus isolation, experiments and/or analyses. D.R., B.L.S., A.L., J.S.A., P.C., G.K., R.R., L.S., and L.S.S. wrote the manuscript. All authors approved the final manuscript.
Competing interests
The authors declare no competing financial interests.
Corresponding authors
Correspondence to Didier Raoult or Bernard La Scola.
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