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Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups

BACKGROUND: The discovery of many fragments of viral genomes integrated in the genome of their eukaryotic host (endogenous viral elements; EVEs) has recently opened new avenues to further our understanding of viral evolution and of host-virus interactions. Here, we report the results of a comprehens...

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Autores principales: Metegnier, Gabriel, Becking, Thomas, Chebbi, Mohamed Amine, Giraud, Isabelle, Moumen, Bouziane, Schaack, Sarah, Cordaux, Richard, Gilbert, Clément
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4573495/
https://www.ncbi.nlm.nih.gov/pubmed/26388953
http://dx.doi.org/10.1186/s13100-015-0047-3
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author Metegnier, Gabriel
Becking, Thomas
Chebbi, Mohamed Amine
Giraud, Isabelle
Moumen, Bouziane
Schaack, Sarah
Cordaux, Richard
Gilbert, Clément
author_facet Metegnier, Gabriel
Becking, Thomas
Chebbi, Mohamed Amine
Giraud, Isabelle
Moumen, Bouziane
Schaack, Sarah
Cordaux, Richard
Gilbert, Clément
author_sort Metegnier, Gabriel
collection PubMed
description BACKGROUND: The discovery of many fragments of viral genomes integrated in the genome of their eukaryotic host (endogenous viral elements; EVEs) has recently opened new avenues to further our understanding of viral evolution and of host-virus interactions. Here, we report the results of a comprehensive screen for EVEs in crustaceans. Following up on the recent discovery of EVEs in the terrestrial isopod, Armadillidium vulgare, we scanned the genomes of six crustacean species: a terrestrial isopod (Armadillidium nasatum), two water fleas (Daphnia pulex and D. pulicaria), two copepods (the salmon louse, Lepeophtheirus salmonis and Eurytemora affinis), and a freshwater amphipod (Hyalella azteca). RESULTS: In total, we found 210 EVEs representing 14 different lineages belonging to five different viral groups that are present in two to five species: Bunyaviridae (−ssRNA), Circoviridae (ssDNA), Mononegavirales (−ssRNA), Parvoviridae (ssDNA) and Totiviridae (dsRNA). The identification of shared orthologous insertions between A. nasatum and A. vulgare indicates that EVEs have been maintained over several millions of years, although we did not find any evidence supporting exaptation. Overall, the different degrees of EVE degradation (from none to >10 nonsense mutations) suggest that endogenization has been recurrent during the evolution of the various crustacean taxa. Our study is the first to report EVEs in D. pulicaria, E. affinis and H. azteca, many of which are likely to result from recent endogenization of currently circulating viruses. CONCLUSIONS: In conclusion, we have unearthed a large diversity of EVEs from crustacean genomes, and shown that four of the five viral groups we uncovered (Bunyaviridae, Circoviridae, Mononegavirales, Parvoviridae) were and may still be present in three to four highly divergent crustacean taxa. In addition, the discovery of recent EVEs offers an interesting opportunity to characterize new exogenous viruses currently circulating in economically or ecologically important copepod species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13100-015-0047-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-45734952015-09-19 Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups Metegnier, Gabriel Becking, Thomas Chebbi, Mohamed Amine Giraud, Isabelle Moumen, Bouziane Schaack, Sarah Cordaux, Richard Gilbert, Clément Mob DNA Research BACKGROUND: The discovery of many fragments of viral genomes integrated in the genome of their eukaryotic host (endogenous viral elements; EVEs) has recently opened new avenues to further our understanding of viral evolution and of host-virus interactions. Here, we report the results of a comprehensive screen for EVEs in crustaceans. Following up on the recent discovery of EVEs in the terrestrial isopod, Armadillidium vulgare, we scanned the genomes of six crustacean species: a terrestrial isopod (Armadillidium nasatum), two water fleas (Daphnia pulex and D. pulicaria), two copepods (the salmon louse, Lepeophtheirus salmonis and Eurytemora affinis), and a freshwater amphipod (Hyalella azteca). RESULTS: In total, we found 210 EVEs representing 14 different lineages belonging to five different viral groups that are present in two to five species: Bunyaviridae (−ssRNA), Circoviridae (ssDNA), Mononegavirales (−ssRNA), Parvoviridae (ssDNA) and Totiviridae (dsRNA). The identification of shared orthologous insertions between A. nasatum and A. vulgare indicates that EVEs have been maintained over several millions of years, although we did not find any evidence supporting exaptation. Overall, the different degrees of EVE degradation (from none to >10 nonsense mutations) suggest that endogenization has been recurrent during the evolution of the various crustacean taxa. Our study is the first to report EVEs in D. pulicaria, E. affinis and H. azteca, many of which are likely to result from recent endogenization of currently circulating viruses. CONCLUSIONS: In conclusion, we have unearthed a large diversity of EVEs from crustacean genomes, and shown that four of the five viral groups we uncovered (Bunyaviridae, Circoviridae, Mononegavirales, Parvoviridae) were and may still be present in three to four highly divergent crustacean taxa. In addition, the discovery of recent EVEs offers an interesting opportunity to characterize new exogenous viruses currently circulating in economically or ecologically important copepod species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13100-015-0047-3) contains supplementary material, which is available to authorized users. BioMed Central 2015-09-16 /pmc/articles/PMC4573495/ /pubmed/26388953 http://dx.doi.org/10.1186/s13100-015-0047-3 Text en © Metegnier et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Metegnier, Gabriel
Becking, Thomas
Chebbi, Mohamed Amine
Giraud, Isabelle
Moumen, Bouziane
Schaack, Sarah
Cordaux, Richard
Gilbert, Clément
Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups
title Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups
title_full Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups
title_fullStr Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups
title_full_unstemmed Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups
title_short Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups
title_sort comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4573495/
https://www.ncbi.nlm.nih.gov/pubmed/26388953
http://dx.doi.org/10.1186/s13100-015-0047-3
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