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      Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel)

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          Abstract

          Background

          Symbiotic bacteria affect insect physiology and ecology. They may also mediate insecticide resistance within their hosts and thereby impact pest and vector control practices. Here, we document a novel mechanism of insecticide resistance in which a gut symbiont of the tephritid pest fruit fly Bactrocera dorsalis enhances resistance to the organophosphate insecticide trichlorphon.

          Results

          We demonstrated that the gut symbiont Citrobacter sp. (CF-BD) plays a key role in the degradation of trichlorphon. Based on a comparative genomics analysis with other Citrobacter species, phosphatase hydrolase genes were identified in CF-BD. These CF-BD genes had higher expression when trichlorphon was present. Bactrocera dorsalis inoculated with isolated CF-BD obtained higher trichlorphon resistance, while antibiotic-treated flies were less resistant confirming the key role of CF-BD in insecticide resistance.

          Conclusions

          Our findings suggest that symbiont-mediated insecticide resistance can readily develop in B. dorsalis and may represent a more widely relevant insecticide resistance mechanism than previously recognized.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s40168-017-0236-z) contains supplementary material, which is available to authorized users.

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          Most cited references67

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          Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.

          mothur aims to be a comprehensive software package that allows users to use a single piece of software to analyze community sequence data. It builds upon previous tools to provide a flexible and powerful software package for analyzing sequencing data. As a case study, we used mothur to trim, screen, and align sequences; calculate distances; assign sequences to operational taxonomic units; and describe the alpha and beta diversity of eight marine samples previously characterized by pyrosequencing of 16S rRNA gene fragments. This analysis of more than 222,000 sequences was completed in less than 2 h with a laptop computer.
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            A Method of Computing the Effectiveness of an Insecticide

            W. Abbott (1925)
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              The gut microbiota of insects - diversity in structure and function.

              Insect guts present distinctive environments for microbial colonization, and bacteria in the gut potentially provide many beneficial services to their hosts. Insects display a wide range in degree of dependence on gut bacteria for basic functions. Most insect guts contain relatively few microbial species as compared to mammalian guts, but some insects harbor large gut communities of specialized bacteria. Others are colonized only opportunistically and sparsely by bacteria common in other environments. Insect digestive tracts vary extensively in morphology and physicochemical properties, factors that greatly influence microbial community structure. One obstacle to the evolution of intimate associations with gut microorganisms is the lack of dependable transmission routes between host individuals. Here, social insects, such as termites, ants, and bees, are exceptions: social interactions provide opportunities for transfer of gut bacteria, and some of the most distinctive and consistent gut communities, with specialized beneficial functions in nutrition and protection, have been found in social insect species. Still, gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication. The extent of these roles is still unclear and awaits further studies. © 2013 Federation of European Microbiological Societies. Published by John Wiley & Sons Ltd. All rights reserved.
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                Author and article information

                Contributors
                +86 2038297715 , xuyijuan@yahoo.com
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                1 February 2017
                1 February 2017
                2017
                : 5
                : 13
                Affiliations
                [1 ]ISNI 0000 0000 9546 5767, GRID grid.20561.30, Department of Entomology, , South China Agricultural University, ; Guangzhou, 510640 China
                [2 ]ISNI 0000 0004 1936 834X, GRID grid.1013.3, Hawkesbury Institute for the Environment, , Western Sydney University, ; Penrith, NSW 2751 Australia
                [3 ]Sun Yat-sen University—Michigan State University Joint Center of Vector Control for Tropical Diseases, Guangzhou, Guangdong 510080 China
                [4 ]ISNI 0000 0001 2150 1785, GRID grid.17088.36, Department of Microbiology and Molecular Genetics, , Michigan State University, ; East Lansing, MI 48824 USA
                Article
                236
                10.1186/s40168-017-0236-z
                5286733
                28143582
                512e5f25-8742-4f7a-8f78-dadc8dd27971
                © The Author(s). 2017

                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.

                History
                : 19 July 2016
                : 24 January 2017
                Funding
                Funded by: the Science Foundation for the Excellent Youth Scholars of Guangdong Province
                Award ID: Yq2013031
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2017

                symbiotic bacteria,insecticide resistance,trichlorphon,bactrocera dorsalis,oriental fruit fly

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