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      Bacterial phylogeny structures soil resistomes across habitats

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          Summary

          Ancient and diverse antibiotic resistance genes (ARGs) have previously been identified from soil 13 , including genes identical to those in human pathogens 4 . Despite the apparent overlap between soil and clinical resistomes 46 , factors influencing ARG composition in soil and their movement between genomes and habitats remain largely unknown 3 . General metagenome functions often correlate with the underlying structure of bacterial communities 712 . However, ARGs are hypothesized to be highly mobile 4, 5, 13 , prompting speculation that resistomes may not correlate with phylogenetic signatures or ecological divisions 13, 14 . To investigate these relationships, we performed functional metagenomic selections for resistance to 18 antibiotics from 18 agricultural and grassland soils. The 2895 ARGs we discovered were predominantly novel, and represent all major resistance mechanisms 15 . We demonstrate that distinct soil types harbor distinct resistomes, and that nitrogen fertilizer amendments strongly influenced soil ARG content. Resistome composition also correlated with microbial phylogenetic and taxonomic structure, both across and within soil types. Consistent with this strong correlation, mobility elements syntenic with ARGs were rare in soil compared to sequenced pathogens, suggesting that ARGs in the soil may not transfer between bacteria as readily as is observed in the clinic. Together, our results indicate that bacterial community composition is the primary determinant of soil ARG content, challenging previous hypotheses that horizontal gene transfer effectively decouples resistomes from phylogeny 13, 14 .

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          Most cited references25

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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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            Call of the wild: antibiotic resistance genes in natural environments.

            Antibiotic-resistant pathogens are profoundly important to human health, but the environmental reservoirs of resistance determinants are poorly understood. The origins of antibiotic resistance in the environment is relevant to human health because of the increasing importance of zoonotic diseases as well as the need for predicting emerging resistant pathogens. This Review explores the presence and spread of antibiotic resistance in non-agricultural, non-clinical environments and demonstrates the need for more intensive investigation on this subject.
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              Cross-biome metagenomic analyses of soil microbial communities and their functional attributes.

              For centuries ecologists have studied how the diversity and functional traits of plant and animal communities vary across biomes. In contrast, we have only just begun exploring similar questions for soil microbial communities despite soil microbes being the dominant engines of biogeochemical cycles and a major pool of living biomass in terrestrial ecosystems. We used metagenomic sequencing to compare the composition and functional attributes of 16 soil microbial communities collected from cold deserts, hot deserts, forests, grasslands, and tundra. Those communities found in plant-free cold desert soils typically had the lowest levels of functional diversity (diversity of protein-coding gene categories) and the lowest levels of phylogenetic and taxonomic diversity. Across all soils, functional beta diversity was strongly correlated with taxonomic and phylogenetic beta diversity; the desert microbial communities were clearly distinct from the nondesert communities regardless of the metric used. The desert communities had higher relative abundances of genes associated with osmoregulation and dormancy, but lower relative abundances of genes associated with nutrient cycling and the catabolism of plant-derived organic compounds. Antibiotic resistance genes were consistently threefold less abundant in the desert soils than in the nondesert soils, suggesting that abiotic conditions, not competitive interactions, are more important in shaping the desert microbial communities. As the most comprehensive survey of soil taxonomic, phylogenetic, and functional diversity to date, this study demonstrates that metagenomic approaches can be used to build a predictive understanding of how microbial diversity and function vary across terrestrial biomes.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                21 May 2014
                21 May 2014
                29 May 2014
                29 November 2014
                : 509
                : 7502
                : 612-616
                Affiliations
                [1 ]Center for Genome Sciences & Systems Biology, Washington University School of Medicine, St. Louis, MO, USA
                [2 ]Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, MO, USA
                [3 ]Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, USA
                [4 ]Department of Chemistry and Biochemistry and BioFrontiers Institute, University of Colorado, Boulder, Colorado, USA
                [5 ]Howard Hughes Medical Institute, Boulder, CO, USA
                [6 ]Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA
                [7 ]Department of Biomedical Engineering, Washington University, St. Louis, MO, USA
                Author notes
                [* ]Correspondence and requests for materials should be addressed to G.D. ( dantas@ 123456wustl.edu )
                [†]

                These authors contributed equally

                Article
                NIHMS587112
                10.1038/nature13377
                4079543
                24847883
                2679a24f-7095-49b5-b189-9db5bfc1b975
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