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      Effects of the Diet on the Microbiota of the Red Palm Weevil (Coleoptera: Dryophthoridae)

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          Abstract

          Rhynchophorus ferrugineus, also known as the red palm weevil, is regarded as the major pest of palm trees. Although studies of the microbiota associated with this species have been performed in recent years, little attention has been dedicated to the influence of the diet in shaping the host bacterial community. Here, we investigated the influence of food sources (i.e. palm tissues vs apple based substrate) on the microbial diversity associated with RPW, which was compared with the microbiota associated with wild individuals of the sister species Rhynchophorus vulneratus. The bacterial characterization was performed using a culture independent approach, i.e. the 16S rRNA pyrotag, and a culture dependent approach for a subset of the samples, in order to obtain bacterial isolates from RPW tissues. The bacterial community appeared significantly influenced by diet. Proteobacteria resulted to be the most abundant clade and was present in all the specimens of the three examined weevil groups. Within Proteobacteria, Enterobacteriaceae were identified in all the organs analysed, including hemolymph and reproductive organs. The apple-fed RPWs and the wild R. vulneratus showed a second dominant taxon within Firmicutes that was scarcely present in the microbiota associated with palm-fed RPWs. A comparative analysis on the bacteria associated with the palm tissues highlighted that 12 bacterial genera out of the 13 identified in the plant tissues were also present in weevils, thus indicating that palm tissues may present a source for bacterial acquisition.

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          Most cited references22

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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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            Antimicrobial peptides keep insect endosymbionts under control.

            Vertically transmitted endosymbionts persist for millions of years in invertebrates and play an important role in animal evolution. However, the functional basis underlying the maintenance of these long-term resident bacteria is unknown. We report that the weevil coleoptericin-A (ColA) antimicrobial peptide selectively targets endosymbionts within the bacteriocytes and regulates their growth through the inhibition of cell division. Silencing the colA gene with RNA interference resulted in a decrease in size of the giant filamentous endosymbionts, which escaped from the bacteriocytes and spread into insect tissues. Although this family of peptides is commonly linked with microbe clearance, this work shows that endosymbiosis benefits from ColA, suggesting that long-term host-symbiont coevolution might have shaped immune effectors for symbiont maintenance.
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              Acetic acid bacteria, newly emerging symbionts of insects.

              Recent research in microbe-insect symbiosis has shown that acetic acid bacteria (AAB) establish symbiotic relationships with several insects of the orders Diptera, Hymenoptera, Hemiptera, and Homoptera, all relying on sugar-based diets, such as nectars, fruit sugars, or phloem sap. To date, the fruit flies Drosophila melanogaster and Bactrocera oleae, mosquitoes of the genera Anopheles and Aedes, the honey bee Apis mellifera, the leafhopper Scaphoideus titanus, and the mealybug Saccharicoccus sacchari have been found to be associated with the bacterial genera Acetobacter, Gluconacetobacter, Gluconobacter, Asaia, and Saccharibacter and the novel genus Commensalibacter. AAB establish symbiotic associations with the insect midgut, a niche characterized by the availability of diet-derived carbohydrates and oxygen and by an acidic pH, selective factors that support AAB growth. AAB have been shown to actively colonize different insect tissues and organs, such as the epithelia of male and female reproductive organs, the Malpighian tubules, and the salivary glands. This complex topology of the symbiosis indicates that AAB possess the keys for passing through body barriers, allowing them to migrate to different organs of the host. Recently, AAB involvement in the regulation of innate immune system homeostasis of Drosophila has been shown, indicating a functional role in host survival. All of these lines of evidence indicate that AAB can play different roles in insect biology, not being restricted to the feeding habit of the host. The close association of AAB and their insect hosts has been confirmed by the demonstration of multiple modes of transmission between individuals and to their progeny that include vertical and horizontal transmission routes, comprising a venereal one. Taken together, the data indicate that AAB represent novel secondary symbionts of insects.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                30 January 2015
                2015
                : 10
                : 1
                : e0117439
                Affiliations
                [1 ]Dipartimento di Scienze Agrarie e Ambientali, Università degli Studi di Milano, Milano, Italy
                [2 ]Dipartimento di Scienze per gli Alimenti, la Nutrizione, l’Ambiente, Università degli Studi di Milano, Milano, Italy
                [3 ]Consiglio per la ricerca e la sperimentazione in agricoltura, Research Centre for Agrobiology and Pedology, Cascine del Riccio, Italy
                [4 ]Dipartimento di Scienze Veterinarie e Sanità Pubblica, Università degli Studi di Milano, Milano, Italy
                [5 ]Dipartimento di Biologia e Biotecnologie “C. Darwin”, Università degli Studi di Roma “La Sapienza”, Roma, Italy
                [6 ]Dipartimento di Gestione dei Sistemi Agroalimentari e Ambientali, Università di Catania, Catania, Italy
                [7 ]Dipartimento di Biologia, Università degli Studi di Firenze, Firenze, Italy
                [8 ]Dipartimento di Scienze Agrarie, Forestali e Alimentari, Università di Torino, Grugliasco, Italy
                [9 ]Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia
                International Atomic Energy Agency, AUSTRIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MM BC. Performed the experiments: MM BC EC EP VV VM ADB GM SL. Analyzed the data: MM BC EC ADB. Contributed reagents/materials/analysis tools: CB DD RC SL AG AA GL. Wrote the paper: MM BC CB DD EC RC GM.

                [¤]

                Current address: Department of Entomology, 5142 Comstock Hall, Cornell University, Ithaca, NY, 14853, United States of America

                ‡ These authors contributed equally to this work.

                Article
                PONE-D-14-47420
                10.1371/journal.pone.0117439
                4311986
                25635833
                8901cfff-2d2a-4691-af4f-f5296ecd222c
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 22 October 2014
                : 23 December 2014
                Page count
                Figures: 6, Tables: 2, Pages: 22
                Funding
                This work was supported by the project BIODESERT GA-245746 “Biotechnology from Desert Microbial Extremophiles for Supporting Agriculture Research Potential in Tunisia and Southern Europe” (European Union), the Prin 2009 (grant 009L27YC8_003) from the Italian Ministry of Education, University and Research (MIUR), Linea B Piano di sviluppo Unimi 2014 (grant 15-6-3) and “Accordo di Programma, affermazione in Edolo del Centro di Eccellenza Università della Montagna” MIUR-Università degli Studi di Milano, prot. n. 1293-05/08/2011. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                Rhynchophorus vulneratus coxI sequences have been deposited at the European Nucleotide Archive with accession numbers LN612634-LN612636. The 16S rRNA gene sequences obtained by 454 pyrosequencing assays were deposited in European Nucleotide Archive with accession numbers PRJEB6918. Partial 16S rRNA gene sequences were deposited in the European Nucleotide Archive under the accession numbers LN623577-LN623640.

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