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      Phylogenomic Study of Burkholderia glathei-like Organisms, Proposal of 13 Novel Burkholderia Species and Emended Descriptions of Burkholderia sordidicola, Burkholderia zhejiangensis, and Burkholderia grimmiae

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          Abstract

          Partial gyrB gene sequence analysis of 17 isolates from human and environmental sources revealed 13 clusters of strains and identified them as Burkholderia glathei clade (BGC) bacteria. The taxonomic status of these clusters was examined by whole-genome sequence analysis, determination of the G+C content, whole-cell fatty acid analysis and biochemical characterization. The whole-genome sequence-based phylogeny was assessed using the Genome Blast Distance Phylogeny (GBDP) method and an extended multilocus sequence analysis (MLSA) approach. The results demonstrated that these 17 BGC isolates represented 13 novel Burkholderia species that could be distinguished by both genotypic and phenotypic characteristics. BGC strains exhibited a broad metabolic versatility and developed beneficial, symbiotic, and pathogenic interactions with different hosts. Our data also confirmed that there is no phylogenetic subdivision in the genus Burkholderia that distinguishes beneficial from pathogenic strains. We therefore propose to formally classify the 13 novel BGC Burkholderia species as Burkholderia arvi sp. nov. (type strain LMG 29317 T = CCUG 68412 T), Burkholderia hypogeia sp. nov. (type strain LMG 29322 T = CCUG 68407 T), Burkholderia ptereochthonis sp. nov. (type strain LMG 29326 T = CCUG 68403 T), Burkholderia glebae sp. nov. (type strain LMG 29325 T = CCUG 68404 T), Burkholderia pedi sp. nov. (type strain LMG 29323 T = CCUG 68406 T), Burkholderia arationis sp. nov. (type strain LMG 29324 T = CCUG 68405 T), Burkholderia fortuita sp. nov. (type strain LMG 29320 T = CCUG 68409 T), Burkholderia temeraria sp. nov. (type strain LMG 29319 T = CCUG 68410 T), Burkholderia calidae sp. nov. (type strain LMG 29321 T = CCUG 68408 T), Burkholderia concitans sp. nov. (type strain LMG 29315 T = CCUG 68414 T), Burkholderia turbans sp. nov. (type strain LMG 29316 T = CCUG 68413 T), Burkholderia catudaia sp. nov. (type strain LMG 29318 T = CCUG 68411 T) and Burkholderia peredens sp. nov. (type strain LMG 29314 T = CCUG 68415 T). Furthermore, we present emended descriptions of the species Burkholderia sordidicola, Burkholderia zhejiangensis and Burkholderia grimmiae. The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA and gyrB gene sequences determined in this study are LT158612-LT158624 and LT158625-LT158641, respectively.

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          Symbiont-mediated insecticide resistance.

          Development of insecticide resistance has been a serious concern worldwide, whose mechanisms have been attributed to evolutionary changes in pest insect genomes such as alteration of drug target sites, up-regulation of degrading enzymes, and enhancement of drug excretion. Here, we report a previously unknown mechanism of insecticide resistance: Infection with an insecticide-degrading bacterial symbiont immediately establishes insecticide resistance in pest insects. The bean bug Riptortus pedestris and allied stinkbugs harbor mutualistic gut symbiotic bacteria of the genus Burkholderia, which are acquired by nymphal insects from environmental soil every generation. In agricultural fields, fenitrothion-degrading Burkolderia strains are present at very low densities. We demonstrated that the fenitrothion-degrading Burkholderia strains establish a specific and beneficial symbiosis with the stinkbugs and confer a resistance of the host insects against fenitrothion. Experimental applications of fenitrothion to field soils drastically enriched fenitrothion-degrading bacteria from undetectable levels to >80% of total culturable bacterial counts in the field soils, and >90% of stinkbugs reared with the enriched soil established symbiosis with fenitrothion-degrading Burkholderia. In a Japanese island where fenitrothion has been constantly applied to sugarcane fields, we identified a stinkbug population wherein the insects live on sugarcane and ≈8% of them host fenitrothion-degrading Burkholderia. Our finding suggests the possibility that the symbiont-mediated insecticide resistance may develop even in the absence of pest insects, quickly establish within a single insect generation, and potentially move around horizontally between different pest insects and other organisms.
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            List of Bacterial Names with Standing in Nomenclature: a folder available on the Internet.

            J Euzéby (1997)
            The List of Bacterial Names with Standing in Nomenclature includes, alphabetically and chronologically, the official names of bacteria as published or validated in the International Journal of Systematic Bacteriology. It encompasses 5,569 taxa (as of 31 December 1996) and is available on the Internet (URL: ftp:@ftp.cict.fr/pub/ bacterio/).
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              An ad hoc committee for the re-evaluation of the species definition in bacteriology met in Gent, Belgium, in February 2002. The committee made various recommendations regarding the species definition in the light of developments in methodologies available to systematists.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                08 June 2016
                2016
                : 7
                : 877
                Affiliations
                [1] 1Laboratory of Microbiology, Department of Biochemistry and Microbiology, Ghent University Ghent, Belgium
                [2] 2Leibniz Institute DSMZ–German Collection of Microorganisms and Cell Cultures GmbH Braunschweig, Germany
                [3] 3Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine Pittsburgh, PA, USA
                [4] 4BCCM/LMG Bacteria Collection, Department of Biochemistry and Microbiology, Ghent University Ghent, Belgium
                Author notes

                Edited by: Martha E. Trujillo, Universidad de Salamanca, Spain

                Reviewed by: Baojun Wu, Wayne State University, USA; Paulina Estrada De Los Santos, Instituto Politecnico Nacional, Mexico

                *Correspondence: Peter Vandamme peter.vandamme@ 123456ugent.be

                This article was submitted to Evolutionary and Genomic Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2016.00877
                4896955
                27375597
                0294e0d9-85e6-45c3-9b50-7aeaaa6aa051
                Copyright © 2016 Peeters, Meier-Kolthoff, Verheyde, De Brandt, Cooper and Vandamme.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 01 April 2016
                : 24 May 2016
                Page count
                Figures: 3, Tables: 5, Equations: 0, References: 94, Pages: 19, Words: 14818
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                burkholderia,genomic taxonomy,gbdp,ggdc,mlsa,phylogenomics
                Microbiology & Virology
                burkholderia, genomic taxonomy, gbdp, ggdc, mlsa, phylogenomics

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