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      The gill-associated microbiome is the main source of wood plant polysaccharide hydrolases and secondary metabolite gene clusters in the mangrove shipworm Neoteredo reynei

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          Abstract

          Teredinidae are a family of highly adapted wood-feeding and wood-boring bivalves, commonly known as shipworms, whose evolution is linked to the acquisition of cellulolytic gammaproteobacterial symbionts harbored in bacteriocytes within the gills. In the present work we applied metagenomics to characterize microbiomes of the gills and digestive tract of Neoteredo reynei, a mangrove-adapted shipworm species found over a large range of the Brazilian coast. Comparative metagenomics grouped the gill symbiont community of different N. reynei specimens, indicating closely related bacterial types are shared. Similarly, the intestine and digestive gland communities were related, yet were more diverse than and showed no overlap with the gill community. Annotation of assembled metagenomic contigs revealed that the gill symbiotic community of N. reynei encodes a plethora of plant cell wall polysaccharides degrading glycoside hydrolase encoding genes, and Biosynthetic Gene Clusters (BGCs). In contrast, the digestive tract microbiomes seem to play little role in wood digestion and secondary metabolites biosynthesis. Metagenome binning recovered the nearly complete genome sequences of two symbiotic Teredinibacter strains from the gills, a representative of Teredinibacter turnerae “clade I” strain, and a yet to be cultivated Teredinibacter sp. type. These Teredinibacter genomes, as well as un-binned gill-derived gammaproteobacteria contigs, also include an endo-β-1,4-xylanase/acetylxylan esterase multi-catalytic carbohydrate-active enzyme, and a trans-acyltransferase polyketide synthase (trans-AT PKS) gene cluster with the gene cassette for generating β-branching on complex polyketides. Finally, we use multivariate analyses to show that the secondary metabolome from the genomes of Teredinibacter representatives, including genomes binned from N. reynei gills’ metagenomes presented herein, stands out within the Cellvibrionaceae family by size, and enrichments for polyketide, nonribosomal peptide and hybrid BGCs. Results presented here add to the growing characterization of shipworm symbiotic microbiomes and indicate that the N. reynei gill gammaproteobacterial community is a prolific source of biotechnologically relevant enzymes for wood-digestion and bioactive compounds production.

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          The comprehensive antibiotic resistance database.

          The field of antibiotic drug discovery and the monitoring of new antibiotic resistance elements have yet to fully exploit the power of the genome revolution. Despite the fact that the first genomes sequenced of free living organisms were those of bacteria, there have been few specialized bioinformatic tools developed to mine the growing amount of genomic data associated with pathogens. In particular, there are few tools to study the genetics and genomics of antibiotic resistance and how it impacts bacterial populations, ecology, and the clinic. We have initiated development of such tools in the form of the Comprehensive Antibiotic Research Database (CARD; http://arpcard.mcmaster.ca). The CARD integrates disparate molecular and sequence data, provides a unique organizing principle in the form of the Antibiotic Resistance Ontology (ARO), and can quickly identify putative antibiotic resistance genes in new unannotated genome sequences. This unique platform provides an informatic tool that bridges antibiotic resistance concerns in health care, agriculture, and the environment.
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              The antibiotic resistome: the nexus of chemical and genetic diversity.

              Over the millennia, microorganisms have evolved evasion strategies to overcome a myriad of chemical and environmental challenges, including antimicrobial drugs. Even before the first clinical use of antibiotics more than 60 years ago, resistant organisms had been isolated. Moreover, the potential problem of the widespread distribution of antibiotic resistant bacteria was recognized by scientists and healthcare specialists from the initial use of these drugs. Why is resistance inevitable and where does it come from? Understanding the molecular diversity that underlies resistance will inform our use of these drugs and guide efforts to develop new efficacious antibiotics.
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                Author and article information

                Contributors
                Role: Formal analysisRole: InvestigationRole: Methodology
                Role: Data curationRole: InvestigationRole: Methodology
                Role: Data curationRole: SoftwareRole: Visualization
                Role: Formal analysis
                Role: Formal analysis
                Role: Software
                Role: InvestigationRole: Resources
                Role: InvestigationRole: Resources
                Role: Software
                Role: Formal analysisRole: SoftwareRole: Visualization
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                14 November 2018
                2018
                : 13
                : 11
                Affiliations
                [1 ] Drug Research and Development Center, Department of Physiology and Pharmacology, Federal University of Ceara, Fortaleza, Ceara, Brazil
                [2 ] Institute of Biology, Federal University of Bahia, Salvador, Bahia, Brazil
                [3 ] Theoretical Biology and Bioinformatics, Utrecht University, Utrecht, Netherlands
                [4 ] Computational Science Research Center, San Diego State University, San Diego, California, United States of America
                [5 ] National Institute of Metrology, Quality and Technology, Rio de Janeiro, Brazil
                [6 ] Centre for Molecular and Biomolecular Informatics, Radboud University Medical Centre, Nijmegen, The Netherlands
                [7 ] National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT IN-TREE), Federal University of Bahia, Salvador, Brazil
                USDA Forest Service, UNITED STATES
                Author notes

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

                Article
                PONE-D-18-18461
                10.1371/journal.pone.0200437
                6235255
                30427852
                © 2018 Brito et al

                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.

                Page count
                Figures: 5, Tables: 1, Pages: 23
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 400764/2014-8
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 473030/2013-6
                Award Recipient :
                This work was supported by the National Counsel of Technological and Scientific Development (CNPq) ( http://cnpq.br) and by the Coordination for the Improvement of Higher Education Personnel (CAPES) ( http://www.capes.gov.br) under the grant numbers 473030/2013-6 and 400764/2014-8 to AETS. BED is supported by Netherlands Organization for Scientific Research (NWO) Vidi grant 864.14.004. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Genetics
                Genomics
                Metagenomics
                Biology and Life Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Biology and Life Sciences
                Species Interactions
                Symbiosis
                Biology and Life Sciences
                Computational Biology
                Genome Analysis
                Biology and Life Sciences
                Genetics
                Genomics
                Genome Analysis
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Digestion
                Medicine and Health Sciences
                Physiology
                Physiological Processes
                Digestion
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbiome
                Biology and Life Sciences
                Genetics
                Genomics
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Microbiology
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Genetics
                Genomics
                Animal Genomics
                Mammalian Genomics
                Biology and Life Sciences
                Organisms
                Bacteria
                Custom metadata
                All metagenomic sequence files are available at ( http://metagenomics.anl.gov) (Metagenomics RAST Server), according the following MG-RAST metagenome IDs: 4603574.3; 4603575.3; 4603576.3; 4603577.3; 4603578.3; 4603579.3; 4603580.3; 4603581.3; 4603582.3; 4603583.3; 4603584.3; 4603585.3; 4603586.3; 4603587.3; 4603579.3. The near genome bins DNA contigs are available at ( http://rast.nmpdr.org) (RAST server) according the following RAST genome IDs 2426.4 and 2426.6.

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