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      Short-term microbial effects of a large-scale mine-tailing storage facility collapse on the local natural environment

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          Abstract

          We investigated the impacts of the Mount Polley tailings impoundment failure on chemical, physical, and microbial properties of substrates within the affected watershed, comprised of 70 hectares of riparian wetlands and 40 km of stream and lake shore. We established a biomonitoring network in October of 2014, two months following the disturbance, and evaluated riparian and wetland substrates for microbial community composition and function via 16S and full metagenome sequencing. A total of 234 samples were collected from substrates at 3 depths and 1,650,752 sequences were recorded in a geodatabase framework. These data revealed a wealth of information regarding watershed-scale distribution of microbial community members, as well as community composition, structure, and response to disturbance. Substrates associated with the impact zone were distinct chemically as indicated by elevated pH, nitrate, and sulphate. The microbial community exhibited elevated metabolic capacity for selenate and sulfate reduction and an abundance of chemolithoautotrophs in the Thiobacillus thiophilus/T. denitrificans/T. thioparus clade that may contribute to nitrate attenuation within the affected watershed. The most impacted area (a 6 km stream connecting two lakes) exhibited 30% lower microbial diversity relative to the remaining sites. The tailings impoundment failure at Mount Polley Mine has provided a unique opportunity to evaluate functional and compositional diversity soon after a major catastrophic disturbance to assess metabolic potential for ecosystem recovery.

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          Most cited references47

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          Diversity in tropical rain forests and coral reefs.

          The commonly observed high diversity of trees in tropical rain forests and corals on tropical reefs is a nonequilibrium state which, if not disturbed further, will progress toward a low-diversity equilibrium community. This may not happen if gradual changes in climate favor different species. If equilibrium is reached, a lesser degree of diversity may be sustained by niche diversification or by a compensatory mortality that favors inferior competitors. However, tropical forests and reefs are subject to severe disturbances often enough that equilibrium may never be attained.
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            Metals, minerals and microbes: geomicrobiology and bioremediation.

            G M Gadd (2010)
            Microbes play key geoactive roles in the biosphere, particularly in the areas of element biotransformations and biogeochemical cycling, metal and mineral transformations, decomposition, bioweathering, and soil and sediment formation. All kinds of microbes, including prokaryotes and eukaryotes and their symbiotic associations with each other and 'higher organisms', can contribute actively to geological phenomena, and central to many such geomicrobial processes are transformations of metals and minerals. Microbes have a variety of properties that can effect changes in metal speciation, toxicity and mobility, as well as mineral formation or mineral dissolution or deterioration. Such mechanisms are important components of natural biogeochemical cycles for metals as well as associated elements in biomass, soil, rocks and minerals, e.g. sulfur and phosphorus, and metalloids, actinides and metal radionuclides. Apart from being important in natural biosphere processes, metal and mineral transformations can have beneficial or detrimental consequences in a human context. Bioremediation is the application of biological systems to the clean-up of organic and inorganic pollution, with bacteria and fungi being the most important organisms for reclamation, immobilization or detoxification of metallic and radionuclide pollutants. Some biominerals or metallic elements deposited by microbes have catalytic and other properties in nanoparticle, crystalline or colloidal forms, and these are relevant to the development of novel biomaterials for technological and antimicrobial purposes. On the negative side, metal and mineral transformations by microbes may result in spoilage and destruction of natural and synthetic materials, rock and mineral-based building materials (e.g. concrete), acid mine drainage and associated metal pollution, biocorrosion of metals, alloys and related substances, and adverse effects on radionuclide speciation, mobility and containment, all with immense social and economic consequences. The ubiquity and importance of microbes in biosphere processes make geomicrobiology one of the most important concepts within microbiology, and one requiring an interdisciplinary approach to define environmental and applied significance and underpin exploitation in biotechnology.
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              Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum.

              Actinobacteria constitute one of the largest phyla among bacteria and represent gram-positive bacteria with a high G+C content in their DNA. This bacterial group includes microorganisms exhibiting a wide spectrum of morphologies, from coccoid to fragmenting hyphal forms, as well as possessing highly variable physiological and metabolic properties. Furthermore, Actinobacteria members have adopted different lifestyles, and can be pathogens (e.g., Corynebacterium, Mycobacterium, Nocardia, Tropheryma, and Propionibacterium), soil inhabitants (Streptomyces), plant commensals (Leifsonia), or gastrointestinal commensals (Bifidobacterium). The divergence of Actinobacteria from other bacteria is ancient, making it impossible to identify the phylogenetically closest bacterial group to Actinobacteria. Genome sequence analysis has revolutionized every aspect of bacterial biology by enhancing the understanding of the genetics, physiology, and evolutionary development of bacteria. Various actinobacterial genomes have been sequenced, revealing a wide genomic heterogeneity probably as a reflection of their biodiversity. This review provides an account of the recent explosion of actinobacterial genomics data and an attempt to place this in a biological and evolutionary context.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: 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
                25 April 2018
                2018
                : 13
                : 4
                : e0196032
                Affiliations
                [1 ] Departments of Natural Resource Sciences & Biological Sciences, Thompson Rivers University, Kamloops, British Columbia, Canada
                [2 ] Department of Chemical and Biological Engineering, University of British Columbia, Vancouver, British Columbia, Canada
                Universita degli Studi di Milano-Bicocca, ITALY
                Author notes

                Competing Interests: Mount Polley Mine Inc provided matching funds, site access, transportation, and material assistance in completing this research project (including protective equipment, boat rental and access, SONDE water quality probes, and access to data/schematics collected by mine employees). This does not alter our adherence to PLOS ONE policies on sharing data and materials.

                [¤]

                Current address: Department of Biology, Covenant College, Lookout Mountain, Georgia, United States of America

                Author information
                http://orcid.org/0000-0003-0416-4128
                Article
                PONE-D-17-36438
                10.1371/journal.pone.0196032
                5918821
                29694379
                71240822-3fd2-4da7-855e-7d2f61a652ae
                © 2018 Garris 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.

                History
                : 10 October 2017
                : 5 April 2018
                Page count
                Figures: 9, Tables: 1, Pages: 25
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004489, Mitacs;
                Award ID: IT03863
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000233, Genome British Columbia;
                Award ID: E01MTP
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000233, Genome British Columbia;
                Award ID: E01MTP
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100008762, Genome Canada;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100008762, Genome Canada;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000038, Natural Sciences and Engineering Research Council of Canada;
                Award ID: EGP 462139 - 13
                Award Recipient :
                Funded by: Mount Polley Mining Corp.
                Award Recipient :
                This project was supported by a Mitacs Accelerate/Elevate Post-doctoral Fellowship for Heath Garris, where professional development seminars/training were provided with little/no input into the content of the research proposal/execution. This program was co-funded by a partner industry (Mount Polley Mining Corp) that contributed substantially to the development of the project (in the form of site access, feasibility assessment, material support, and manuscript review). Additional funding from NSERC was awarded to support an initial (pre-breach) water quality project. NSERC monitored changes in the proposed project scope by requesting reports, but did not contribute to the content of the study directly. Finally, Genome BC and Genome Canada supported the project through funding and consultation on project scope/applicability/suitability with respect to the use of genomics technologies and accomplishment of project goals, which served to improve project precisions/outcomes. Project funding web references: Mitacs ( https://www.mitacs.ca/en/impact/postdoctoral-fellows-share-program-benefits-mitacs-elevate-retreat); Genome BC ( https://www.genomecanada.ca/en/metagenomics-assess-impacts-mount-polley-mine-taillings-dam-breach-associated-ecosystems); Genome Canada ( https://www.genomecanada.ca/en/metagenomics-assess-impacts-mount-polley-mine-taillings-dam-breach-associated-ecosystems); Mount Polley Mine ( https://www.imperialmetals.com/assets/docs/mt-polley/2015-02-23_MPFN.pdf).
                Categories
                Research Article
                Earth Sciences
                Marine and Aquatic Sciences
                Bodies of Water
                Lakes
                Ecology and Environmental Sciences
                Aquatic Environments
                Freshwater Environments
                Lakes
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Freshwater Environments
                Lakes
                Earth Sciences
                Geology
                Petrology
                Sediment
                Earth Sciences
                Geology
                Sedimentary Geology
                Sediment
                Physical Sciences
                Chemistry
                Chemical Compounds
                Salts
                Sulfates
                Biology and Life Sciences
                Ecology
                Community Ecology
                Community Structure
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Community Structure
                Earth Sciences
                Hydrology
                Surface Water
                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
                Ecology
                Ecological Metrics
                Species Diversity
                Ecology and Environmental Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Earth Sciences
                Geomorphology
                Topography
                Landforms
                Shores
                Custom metadata
                All sequence data are available at https://www.ncbi.nlm.nih.gov/, project number PRJNA433688. Metadata are available at http://www.datadryad.org/, accession DOI: https://doi.org/10.5061/dryad.d52df21.

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