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

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          Abstract

          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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          Most cited references60

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          Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera.

          A Douglas (1998)
          Most aphids possess intracellular bacteria of the genus Buchnera. The bacteria are transmitted vertically via the aphid ovary, and the association is obligate for both partners: Bacteria-free aphids grow poorly and produce few or no offspring, and Buchnera are both unknown apart from aphids and apparently unculturable. The symbiosis has a nutritional basis. Specifically, bacterial provisioning of essential amino acids has been demonstrated. Nitrogen recycling, however, is not quantitatively important to the nutrition of aphid species studied, and there is strong evidence against bacterial involvement in the lipid and sterol nutrition of aphids. Buchnera have been implicated in various non-nutritional functions. Of these, just one has strong experimental support: promotion of aphid transmission of circulative viruses. It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.
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            Learning how to live together: genomic insights into prokaryote-animal symbioses.

            Our understanding of prokaryote-eukaryote symbioses as a source of evolutionary innovation has been rapidly increased by the advent of genomics, which has made possible the biological study of uncultivable endosymbionts. Genomics is allowing the dissection of the evolutionary process that starts with host invasion then progresses from facultative to obligate symbiosis and ends with replacement by, or coexistence with, new symbionts. Moreover, genomics has provided important clues on the mechanisms driving the genome-reduction process, the functions that are retained by the endosymbionts, the role of the host, and the factors that might determine whether the association will become parasitic or mutualistic.
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              The Pathway Tools software.

              Bioinformatics requires reusable software tools for creating model-organism databases (MODs). The Pathway Tools is a reusable, production-quality software environment for creating a type of MOD called a Pathway/Genome Database (PGDB). A PGDB such as EcoCyc (see http://ecocyc.org) integrates our evolving understanding of the genes, proteins, metabolic network, and genetic network of an organism. This paper provides an overview of the four main components of the Pathway Tools: The PathoLogic component supports creation of new PGDBs from the annotated genome of an organism. The Pathway/Genome Navigator provides query, visualization, and Web-publishing services for PGDBs. The Pathway/Genome Editors support interactive updating of PGDBs. The Pathway Tools ontology defines the schema of PGDBs. The Pathway Tools makes use of the Ocelot object database system for data management services for PGDBs. The Pathway Tools has been used to build PGDBs for 13 organisms within SRI and by external users.
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                Author and article information

                Contributors
                qiong.rao@163.com
                pierre-antoine.farnier@univ-lyon1.fr
                zjwzzdt@163.com
                Diego.Santos@uv.es
                francisco.silva@uv.es
                Andres.Moya@uv.es
                amparo.latorre@uv.es
                Cecilia.Coimbra-Klein@univ-lyon1.fr
                Fabrice.Vavre@univ-lyon1.fr
                marie-france.sagot@inria.fr
                shshliu@zju.edu.cn
                laurence.mouton@univ-lyon1.fr
                xwwang@zju.edu.cn
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                21 March 2015
                21 March 2015
                2015
                : 16
                : 1
                : 226
                Affiliations
                [ ]Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, 310058 Hangzhou, China
                [ ]Université de Lyon, Université Lyon1, Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 558, 69622 Villeurbanne, Cedex France
                [ ]Inria Grenoble Rhône-Alpes, Grenoble, France
                [ ]Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, Valencia, Spain
                [ ]Unidad Mixta de Investigación en Genómica y Salud FISABIO-Salud Pública and Universitat de València, Valencia, Spain
                [ ]School of Agriculture and Food Science, Zhejiang A & F University, 311300 Lin’an, Zhejiang China
                Article
                1379
                10.1186/s12864-015-1379-6
                4438442
                25887812
                8a70216e-2484-475c-89f3-ef41b40fbbc6
                © 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.

                History
                : 18 September 2014
                : 21 February 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Genetics
                endosymbiont,genome,hamiltonella,portiera,whitefly,metabolic complementation
                Genetics
                endosymbiont, genome, hamiltonella, portiera, whitefly, metabolic complementation

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