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A metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts
BACKGROUND: Aphids are known to live in symbiosis with specific bacteria, called endosymbionts which can be classified as obligate or accessory. Buchnera aphidicola is generally the only obligatory symbiont present in aphids, supplying essential nutrients that are missing in the plants phloem to its...
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/PMC4678535/ https://www.ncbi.nlm.nih.gov/pubmed/26667400 http://dx.doi.org/10.1186/s40168-015-0130-5 |
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author | De Clerck, Caroline Fujiwara, Akiko Joncour, Pauline Léonard, Simon Félix, Marie-Line Francis, Frédéric Jijakli, M. Haissam Tsuchida, Tsutomu Massart, Sébastien |
author_facet | De Clerck, Caroline Fujiwara, Akiko Joncour, Pauline Léonard, Simon Félix, Marie-Line Francis, Frédéric Jijakli, M. Haissam Tsuchida, Tsutomu Massart, Sébastien |
author_sort | De Clerck, Caroline |
collection | PubMed |
description | BACKGROUND: Aphids are known to live in symbiosis with specific bacteria, called endosymbionts which can be classified as obligate or accessory. Buchnera aphidicola is generally the only obligatory symbiont present in aphids, supplying essential nutrients that are missing in the plants phloem to its host. Pentalonia nigronervosa is the main vector of the banana bunchy top virus, one of the most damageable viruses in banana. This aphid is carrying two symbionts: B. aphidicola (BPn) and Wolbachia sp. (wPn). The high occurrence of Wolbachia in the banana aphid raises questions about the role it plays in this insect. The goal of this study was to go further in the understanding of the role played by the two symbionts in P. nigronervosa. To do so, microinjection tests were made to see the effect of wPn elimination on the host, and then, high-throughput sequencing of the haemolymph was used to analyze the gene content of the symbionts. RESULTS: We observed that the elimination of wPn systematically led to the death of aphids, suggesting that the bacterium could play a mutualistic role. In addition, we identify and annotate 587 and 250 genes for wPn and BPn, respectively, through high-throughput sequencing. Analysis of these genes suggests that the two bacteria are working together for the production of several essential nutrients. The most striking cases are for lysin and riboflavin which are usually provided by B. aphidicola alone to the host. In the banana aphid, the genes involved in the production pathways of these metabolites are shared between the two bacteria making them both essential for the survival of the aphid host. CONCLUSIONS: Our results suggest that a co-obligatory symbiosis between B. aphidicola and Wolbachia occurs in the banana aphid, the two bacteria acting together to supply essential nutrients to the host. This is, to our knowledge, the first time Wolbachia is reported to play an essential role in aphids. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40168-015-0130-5) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4678535 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-46785352015-12-16 A metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts De Clerck, Caroline Fujiwara, Akiko Joncour, Pauline Léonard, Simon Félix, Marie-Line Francis, Frédéric Jijakli, M. Haissam Tsuchida, Tsutomu Massart, Sébastien Microbiome Research BACKGROUND: Aphids are known to live in symbiosis with specific bacteria, called endosymbionts which can be classified as obligate or accessory. Buchnera aphidicola is generally the only obligatory symbiont present in aphids, supplying essential nutrients that are missing in the plants phloem to its host. Pentalonia nigronervosa is the main vector of the banana bunchy top virus, one of the most damageable viruses in banana. This aphid is carrying two symbionts: B. aphidicola (BPn) and Wolbachia sp. (wPn). The high occurrence of Wolbachia in the banana aphid raises questions about the role it plays in this insect. The goal of this study was to go further in the understanding of the role played by the two symbionts in P. nigronervosa. To do so, microinjection tests were made to see the effect of wPn elimination on the host, and then, high-throughput sequencing of the haemolymph was used to analyze the gene content of the symbionts. RESULTS: We observed that the elimination of wPn systematically led to the death of aphids, suggesting that the bacterium could play a mutualistic role. In addition, we identify and annotate 587 and 250 genes for wPn and BPn, respectively, through high-throughput sequencing. Analysis of these genes suggests that the two bacteria are working together for the production of several essential nutrients. The most striking cases are for lysin and riboflavin which are usually provided by B. aphidicola alone to the host. In the banana aphid, the genes involved in the production pathways of these metabolites are shared between the two bacteria making them both essential for the survival of the aphid host. CONCLUSIONS: Our results suggest that a co-obligatory symbiosis between B. aphidicola and Wolbachia occurs in the banana aphid, the two bacteria acting together to supply essential nutrients to the host. This is, to our knowledge, the first time Wolbachia is reported to play an essential role in aphids. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40168-015-0130-5) contains supplementary material, which is available to authorized users. BioMed Central 2015-12-15 /pmc/articles/PMC4678535/ /pubmed/26667400 http://dx.doi.org/10.1186/s40168-015-0130-5 Text en © De Clerck 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 De Clerck, Caroline Fujiwara, Akiko Joncour, Pauline Léonard, Simon Félix, Marie-Line Francis, Frédéric Jijakli, M. Haissam Tsuchida, Tsutomu Massart, Sébastien A metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts |
title | A metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts |
title_full | A metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts |
title_fullStr | A metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts |
title_full_unstemmed | A metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts |
title_short | A metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts |
title_sort | metagenomic approach from aphid’s hemolymph sheds light on the potential roles of co-existing endosymbionts |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4678535/ https://www.ncbi.nlm.nih.gov/pubmed/26667400 http://dx.doi.org/10.1186/s40168-015-0130-5 |
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