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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...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2015
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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. |
format | Online Article Text |
id | pubmed-4573495 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
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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