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      The selective pressures on the microbial community in a metal-contaminated aquifer

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          Abstract

          In many environments, toxic compounds restrict which microorganisms persist. However, in complex mixtures of inhibitory compounds, it is challenging to determine which specific compounds cause changes in abundance and prevent some microorganisms from growing. We focused on a contaminated aquifer in Oak Ridge, Tennessee, USA that has large gradients of pH and widely varying concentrations of uranium, nitrate, and many other inorganic ions. In the most contaminated wells, the microbial community is enriched in the Rhodanobacter genus. Rhodanobacter abundance is positively correlated with low pH and high concentrations of uranium and 13 other ions and we sought to determine which of these ions are selective pressures that favor the growth of Rhodanobacter over other taxa. Of these ions, low pH and high UO 2 2+, Mn 2+, Al 3+, Cd 2+, Zn 2+, Co 2+, and Ni 2+ are both (a) selectively inhibitory of a Pseudomonas isolate from an uncontaminated well vs. a Rhodanobacter isolate from a contaminated well, and (b) reach toxic concentrations (for the Pseudomonas isolate) in the Rhodanobacter-dominated wells. We used mixtures of ions to simulate the groundwater conditions in the most contaminated wells and verified that few isolates aside from Rhodanobacter can tolerate these eight ions. These results clarify which ions are likely causal factors that impact the microbial community at this field site and are not merely correlated with taxonomic shifts. Furthermore, our general high-throughput approach can be applied to other environments, isolates, and conditions to systematically help identify selective pressures on microbial communities.

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          Most cited references40

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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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            The “North American shale composite”: Its compilation, major and trace element characteristics

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                Author and article information

                Contributors
                HKCarlson@lbl.gov
                AMDeutschbauer@lbl.gov
                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group UK (London )
                1751-7362
                1751-7370
                6 December 2018
                6 December 2018
                April 2019
                : 13
                : 4
                : 937-949
                Affiliations
                [1 ]ISNI 0000 0001 2231 4551, GRID grid.184769.5, Environmental Genomics and Systems Biology Division, , Lawrence Berkeley National Laboratory, ; Berkeley, CA 94720 USA
                [2 ]ISNI 0000 0001 2231 4551, GRID grid.184769.5, Earth and Environmental Sciences Area, , Lawrence Berkeley National Laboratory, ; Berkeley, CA 94720 USA
                [3 ]ISNI 0000 0001 2181 7878, GRID grid.47840.3f, Department of Bioengineering, , University of California, ; Berkeley, CA 94720 USA
                [4 ]ISNI 0000 0001 2181 7878, GRID grid.47840.3f, Department of Plant and Microbial Biology, , University of California, ; Berkeley, CA 94720 USA
                Author information
                http://orcid.org/0000-0001-9326-554X
                Article
                328
                10.1038/s41396-018-0328-1
                6461962
                30523276
                0ee66379-6bd8-4531-ad84-b8e2abbcab3c
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 10 September 2018
                : 12 November 2018
                : 22 November 2018
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000015, U.S. Department of Energy (DOE);
                Award ID: DE-AC02-05CH11231
                Award ID: DE-AC02-05CH11231
                Award ID: DE-AC02-05CH11231
                Award ID: DE-AC02-05CH11231
                Award ID: DE-AC02-05CH11231
                Award ID: DE-AC02-05CH11231
                Award ID: DE-AC02-05CH11231
                Award Recipient :
                Categories
                Article
                Custom metadata
                © International Society for Microbial Ecology 2019

                Microbiology & Virology
                microbial ecology,environmental chemistry
                Microbiology & Virology
                microbial ecology, environmental chemistry

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