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      A reservoir of ‘historical’ antibiotic resistance genes in remote pristine Antarctic soils

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          Abstract

          Background

          Soil bacteria naturally produce antibiotics as a competitive mechanism, with a concomitant evolution, and exchange by horizontal gene transfer, of a range of antibiotic resistance mechanisms. Surveys of bacterial resistance elements in edaphic systems have originated primarily from human-impacted environments, with relatively little information from remote and pristine environments, where the resistome may comprise the ancestral gene diversity.

          Methods

          We used shotgun metagenomics to assess antibiotic resistance gene (ARG) distribution in 17 pristine and remote Antarctic surface soils within the undisturbed Mackay Glacier region. We also interrogated the phylogenetic placement of ARGs compared to environmental ARG sequences and tested for the presence of horizontal gene transfer elements flanking ARGs.

          Results

          In total, 177 naturally occurring ARGs were identified, most of which encoded single or multi-drug efflux pumps. Resistance mechanisms for the inactivation of aminoglycosides, chloramphenicol and β-lactam antibiotics were also common. Gram-negative bacteria harboured most ARGs (71%), with fewer genes from Gram-positive Actinobacteria and Bacilli ( Firmicutes) (9%), reflecting the taxonomic composition of the soils. Strikingly, the abundance of ARGs per sample had a strong, negative correlation with species richness ( r = − 0.49, P < 0.05). This result, coupled with a lack of mobile genetic elements flanking ARGs, suggests that these genes are ancient acquisitions of horizontal transfer events.

          Conclusions

          ARGs in these remote and uncontaminated soils most likely represent functional efficient historical genes that have since been vertically inherited over generations. The historical ARGs in these pristine environments carry a strong phylogenetic signal and form a monophyletic group relative to ARGs from other similar environments.

          Electronic supplementary material

          The online version of this article (10.1186/s40168-018-0424-5) contains supplementary material, which is available to authorized users.

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          Most cited references42

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          FLASH: fast length adjustment of short reads to improve genome assemblies.

          Next-generation sequencing technologies generate very large numbers of short reads. Even with very deep genome coverage, short read lengths cause problems in de novo assemblies. The use of paired-end libraries with a fragment size shorter than twice the read length provides an opportunity to generate much longer reads by overlapping and merging read pairs before assembling a genome. We present FLASH, a fast computational tool to extend the length of short reads by overlapping paired-end reads from fragment libraries that are sufficiently short. We tested the correctness of the tool on one million simulated read pairs, and we then applied it as a pre-processor for genome assemblies of Illumina reads from the bacterium Staphylococcus aureus and human chromosome 14. FLASH correctly extended and merged reads >99% of the time on simulated reads with an error rate of <1%. With adequately set parameters, FLASH correctly merged reads over 90% of the time even when the reads contained up to 5% errors. When FLASH was used to extend reads prior to assembly, the resulting assemblies had substantially greater N50 lengths for both contigs and scaffolds. The FLASH system is implemented in C and is freely available as open-source code at http://www.cbcb.umd.edu/software/flash. t.magoc@gmail.com.
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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

                Contributors
                +27 12 420 6976 , Thulani.makhalanyane@up.ac.za
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                23 February 2018
                23 February 2018
                2018
                : 6
                : 40
                Affiliations
                [1 ]ISNI 0000 0001 2107 2298, GRID grid.49697.35, Centre for Microbial Ecology and Genomics (CMEG), Department of Biochemistry, Genetics and Microbiology, , University of Pretoria, ; Natural Sciences Building 2, Lynnwood Road, Pretoria, 0028 South Africa
                [2 ]ISNI 0000 0001 2107 2298, GRID grid.49697.35, Centre for Bioinformatics and Computational Biology, Department of Biochemistry, Genetics and Microbiology, , University of Pretoria, ; Pretoria, South Africa
                [3 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Department of Plant Biotechnology and Bioinformatics, , Ghent University, ; 9052 Ghent, Belgium
                [4 ]ISNI 0000000104788040, GRID grid.11486.3a, Center for Plant Systems Biology, VIB, ; 9052 Ghent, Belgium
                [5 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Bioinformatics Institute Ghent, , Ghent University, ; 9052 Ghent, Belgium
                Author information
                http://orcid.org/0000-0002-8173-1678
                Article
                424
                10.1186/s40168-018-0424-5
                5824556
                29471872
                1a26252a-bc57-4f3d-a35f-08a3005b9d3c
                © The Author(s). 2018

                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
                : 22 November 2017
                : 11 February 2018
                Funding
                Funded by: National Research Foundation of South Africa
                Award ID: 93074
                Award ID: 97891
                Award ID: 99320
                Funded by: FundRef http://dx.doi.org/10.13039/501100001321, National Research Foundation;
                Award ID: 110717
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                antibiotic resistance genes,soil resistome,antarctica,metagenomics

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