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Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci

BACKGROUND: The whitefly Bemisia tabaci is an important agricultural pest with global distribution. This phloem-sap feeder harbors a primary symbiont, “Candidatus Portiera aleyrodidarum”, which compensates for the deficient nutritional composition of its food sources, and a variety of secondary symb...

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Autores principales: Rao, Qiong, Rollat-Farnier, Pierre-Antoine, Zhu, Dan-Tong, Santos-Garcia, Diego, Silva, Francisco J, Moya, Andrés, Latorre, Amparo, Klein, Cecilia C, Vavre, Fabrice, Sagot, Marie-France, Liu, Shu-Sheng, Mouton, Laurence, Wang, Xiao-Wei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4438442/
https://www.ncbi.nlm.nih.gov/pubmed/25887812
http://dx.doi.org/10.1186/s12864-015-1379-6
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author Rao, Qiong
Rollat-Farnier, Pierre-Antoine
Zhu, Dan-Tong
Santos-Garcia, Diego
Silva, Francisco J
Moya, Andrés
Latorre, Amparo
Klein, Cecilia C
Vavre, Fabrice
Sagot, Marie-France
Liu, Shu-Sheng
Mouton, Laurence
Wang, Xiao-Wei
author_facet Rao, Qiong
Rollat-Farnier, Pierre-Antoine
Zhu, Dan-Tong
Santos-Garcia, Diego
Silva, Francisco J
Moya, Andrés
Latorre, Amparo
Klein, Cecilia C
Vavre, Fabrice
Sagot, Marie-France
Liu, Shu-Sheng
Mouton, Laurence
Wang, Xiao-Wei
author_sort Rao, Qiong
collection PubMed
description BACKGROUND: The whitefly Bemisia tabaci is an important agricultural pest with global distribution. This phloem-sap feeder harbors a primary symbiont, “Candidatus Portiera aleyrodidarum”, which compensates for the deficient nutritional composition of its food sources, and a variety of secondary symbionts. Interestingly, all of these secondary symbionts are found in co-localization with the primary symbiont within the same bacteriocytes, which should favor the evolution of strong interactions between symbionts. RESULTS: In this paper, we analyzed the genome sequences of the primary symbiont Portiera and of the secondary symbiont Hamiltonella in the B. tabaci Mediterranean (MED) species in order to gain insight into the metabolic role of each symbiont in the biology of their host. The genome sequences of the uncultured symbionts Portiera and Hamiltonella were obtained from one single bacteriocyte of MED B. tabaci. As already reported, the genome of Portiera is highly reduced (357 kb), but has kept a number of genes encoding most essential amino-acids and carotenoids. On the other hand, Portiera lacks almost all the genes involved in the synthesis of vitamins and cofactors. Moreover, some pathways are incomplete, notably those involved in the synthesis of some essential amino-acids. Interestingly, the genome of Hamiltonella revealed that this secondary symbiont can not only provide vitamins and cofactors, but also complete the missing steps of some of the pathways of Portiera. In addition, some critical amino-acid biosynthetic genes are missing in the two symbiotic genomes, but analysis of whitefly transcriptome suggests that the missing steps may be performed by the whitefly itself or its microbiota. CONCLUSIONS: These data suggest that Portiera and Hamiltonella are not only complementary but could also be mutually dependent to provide a full complement of nutrients to their host. Altogether, these results illustrate how functional redundancies can lead to gene losses in the genomes of the different symbiotic partners, reinforcing their inter-dependency. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1379-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-44384422015-05-21 Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci Rao, Qiong Rollat-Farnier, Pierre-Antoine Zhu, Dan-Tong Santos-Garcia, Diego Silva, Francisco J Moya, Andrés Latorre, Amparo Klein, Cecilia C Vavre, Fabrice Sagot, Marie-France Liu, Shu-Sheng Mouton, Laurence Wang, Xiao-Wei BMC Genomics Research Article BACKGROUND: The whitefly Bemisia tabaci is an important agricultural pest with global distribution. This phloem-sap feeder harbors a primary symbiont, “Candidatus Portiera aleyrodidarum”, which compensates for the deficient nutritional composition of its food sources, and a variety of secondary symbionts. Interestingly, all of these secondary symbionts are found in co-localization with the primary symbiont within the same bacteriocytes, which should favor the evolution of strong interactions between symbionts. RESULTS: In this paper, we analyzed the genome sequences of the primary symbiont Portiera and of the secondary symbiont Hamiltonella in the B. tabaci Mediterranean (MED) species in order to gain insight into the metabolic role of each symbiont in the biology of their host. The genome sequences of the uncultured symbionts Portiera and Hamiltonella were obtained from one single bacteriocyte of MED B. tabaci. As already reported, the genome of Portiera is highly reduced (357 kb), but has kept a number of genes encoding most essential amino-acids and carotenoids. On the other hand, Portiera lacks almost all the genes involved in the synthesis of vitamins and cofactors. Moreover, some pathways are incomplete, notably those involved in the synthesis of some essential amino-acids. Interestingly, the genome of Hamiltonella revealed that this secondary symbiont can not only provide vitamins and cofactors, but also complete the missing steps of some of the pathways of Portiera. In addition, some critical amino-acid biosynthetic genes are missing in the two symbiotic genomes, but analysis of whitefly transcriptome suggests that the missing steps may be performed by the whitefly itself or its microbiota. CONCLUSIONS: These data suggest that Portiera and Hamiltonella are not only complementary but could also be mutually dependent to provide a full complement of nutrients to their host. Altogether, these results illustrate how functional redundancies can lead to gene losses in the genomes of the different symbiotic partners, reinforcing their inter-dependency. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1379-6) contains supplementary material, which is available to authorized users. BioMed Central 2015-03-21 /pmc/articles/PMC4438442/ /pubmed/25887812 http://dx.doi.org/10.1186/s12864-015-1379-6 Text en © Rao et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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
Rao, Qiong
Rollat-Farnier, Pierre-Antoine
Zhu, Dan-Tong
Santos-Garcia, Diego
Silva, Francisco J
Moya, Andrés
Latorre, Amparo
Klein, Cecilia C
Vavre, Fabrice
Sagot, Marie-France
Liu, Shu-Sheng
Mouton, Laurence
Wang, Xiao-Wei
Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci
title Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci
title_full Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci
title_fullStr Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci
title_full_unstemmed Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci
title_short Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci
title_sort genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly bemisia tabaci
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4438442/
https://www.ncbi.nlm.nih.gov/pubmed/25887812
http://dx.doi.org/10.1186/s12864-015-1379-6
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