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Mariner transposons are sailing in the genome of the blood-sucking bug Rhodnius prolixus

BACKGROUND: The Triatomine bug Rhodnius prolixus is a vector of Trypanosoma cruzi, which causes the Chagas disease in Latin America. R. prolixus can also transfer transposable elements horizontally across a wide range of species. We have taken advantage of the availability of the 700 Mbp complete ge...

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Autores principales: Filée, Jonathan, Rouault, Jacques-Deric, Harry, Myriam, Hua-Van, Aurélie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4678618/
https://www.ncbi.nlm.nih.gov/pubmed/26666222
http://dx.doi.org/10.1186/s12864-015-2060-9
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author Filée, Jonathan
Rouault, Jacques-Deric
Harry, Myriam
Hua-Van, Aurélie
author_facet Filée, Jonathan
Rouault, Jacques-Deric
Harry, Myriam
Hua-Van, Aurélie
author_sort Filée, Jonathan
collection PubMed
description BACKGROUND: The Triatomine bug Rhodnius prolixus is a vector of Trypanosoma cruzi, which causes the Chagas disease in Latin America. R. prolixus can also transfer transposable elements horizontally across a wide range of species. We have taken advantage of the availability of the 700 Mbp complete genome sequence of R. prolixus to study the dynamics of invasion and persistence of transposable elements in this species. RESULTS: Using both library-based and de novo methods of transposon detection, we found less than 6 % of transposable elements in the R. prolixus genome, a relatively low percentage compared to other insect genomes with a similar genome size. DNA transposons are surprisingly abundant and elements belonging to the mariner family are by far the most preponderant components of the mobile part of this genome with 11,015 mariner transposons that could be clustered in 89 groups (75 % of the mobilome). Our analysis allowed the detection of a new mariner clade in the R. prolixus genome, that we called nosferatis. We demonstrated that a large diversity of mariner elements invaded the genome and expanded successfully over time via three main processes. (i) several families experienced recent and massive expansion, for example an explosive burst of a single mariner family led to the generation of more than 8000 copies. These recent expansion events explain the unusual prevalence of mariner transposons in the R. prolixus genome. Other families expanded via older bursts of transposition demonstrating the long lasting permissibility of mariner transposons in the R. prolixus genome. (ii) Many non-autonomous families generated by internal deletions were also identified. Interestingly, two non autonomous families were generated by atypical recombinations (5' part replacement with 3' part). (iii) at least 10 cases of horizontal transfers were found, supporting the idea that host/vector relationships played a pivotal role in the transmission and subsequent persistence of transposable elements in this genome. CONCLUSION: These data provide a new insight into the evolution of transposons in the genomes of hematophagous insects and bring additional evidences that lateral exchanges of mobile genetics elements occur frequently in the R. prolixus genome. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-2060-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-46786182015-12-16 Mariner transposons are sailing in the genome of the blood-sucking bug Rhodnius prolixus Filée, Jonathan Rouault, Jacques-Deric Harry, Myriam Hua-Van, Aurélie BMC Genomics Research Article BACKGROUND: The Triatomine bug Rhodnius prolixus is a vector of Trypanosoma cruzi, which causes the Chagas disease in Latin America. R. prolixus can also transfer transposable elements horizontally across a wide range of species. We have taken advantage of the availability of the 700 Mbp complete genome sequence of R. prolixus to study the dynamics of invasion and persistence of transposable elements in this species. RESULTS: Using both library-based and de novo methods of transposon detection, we found less than 6 % of transposable elements in the R. prolixus genome, a relatively low percentage compared to other insect genomes with a similar genome size. DNA transposons are surprisingly abundant and elements belonging to the mariner family are by far the most preponderant components of the mobile part of this genome with 11,015 mariner transposons that could be clustered in 89 groups (75 % of the mobilome). Our analysis allowed the detection of a new mariner clade in the R. prolixus genome, that we called nosferatis. We demonstrated that a large diversity of mariner elements invaded the genome and expanded successfully over time via three main processes. (i) several families experienced recent and massive expansion, for example an explosive burst of a single mariner family led to the generation of more than 8000 copies. These recent expansion events explain the unusual prevalence of mariner transposons in the R. prolixus genome. Other families expanded via older bursts of transposition demonstrating the long lasting permissibility of mariner transposons in the R. prolixus genome. (ii) Many non-autonomous families generated by internal deletions were also identified. Interestingly, two non autonomous families were generated by atypical recombinations (5' part replacement with 3' part). (iii) at least 10 cases of horizontal transfers were found, supporting the idea that host/vector relationships played a pivotal role in the transmission and subsequent persistence of transposable elements in this genome. CONCLUSION: These data provide a new insight into the evolution of transposons in the genomes of hematophagous insects and bring additional evidences that lateral exchanges of mobile genetics elements occur frequently in the R. prolixus genome. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-2060-9) contains supplementary material, which is available to authorized users. BioMed Central 2015-12-15 /pmc/articles/PMC4678618/ /pubmed/26666222 http://dx.doi.org/10.1186/s12864-015-2060-9 Text en © Filée 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 Article
Filée, Jonathan
Rouault, Jacques-Deric
Harry, Myriam
Hua-Van, Aurélie
Mariner transposons are sailing in the genome of the blood-sucking bug Rhodnius prolixus
title Mariner transposons are sailing in the genome of the blood-sucking bug Rhodnius prolixus
title_full Mariner transposons are sailing in the genome of the blood-sucking bug Rhodnius prolixus
title_fullStr Mariner transposons are sailing in the genome of the blood-sucking bug Rhodnius prolixus
title_full_unstemmed Mariner transposons are sailing in the genome of the blood-sucking bug Rhodnius prolixus
title_short Mariner transposons are sailing in the genome of the blood-sucking bug Rhodnius prolixus
title_sort mariner transposons are sailing in the genome of the blood-sucking bug rhodnius prolixus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4678618/
https://www.ncbi.nlm.nih.gov/pubmed/26666222
http://dx.doi.org/10.1186/s12864-015-2060-9
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