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      Insights from the Metagenome of an Acid Salt Lake: The Role of Biology in an Extreme Depositional Environment

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          Abstract

          The extremely acidic brine lakes of the Yilgarn Craton of Western Australia are home to some of the most biologically challenging waters on Earth. In this study, we employed metagenomic shotgun sequencing to generate a microbial profile of the depositional environment associated with the sulfur-rich sediments of one such lake. Of the 1.5 M high-quality reads generated, 0.25 M were mapped to protein features, which in turn provide new insights into the metabolic function of this community. In particular, 45 diverse genes associated with sulfur metabolism were identified, the majority of which were linked to either the conversion of sulfate to adenylylsulfate and the subsequent production of sulfide from sulfite or the oxidation of sulfide, elemental sulfur, and thiosulfate via the sulfur oxidation (Sox) system. This is the first metagenomic study of an acidic, hypersaline depositional environment, and we present evidence for a surprisingly high level of microbial diversity. Our findings also illuminate the possibility that we may be meaningfully underestimating the effects of biology on the chemistry of these sulfur-rich sediments, thereby influencing our understanding of past geobiological conditions that may have been present on Earth as well as early Mars.

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          Global mineralogical and aqueous mars history derived from OMEGA/Mars Express data.

          Global mineralogical mapping of Mars by the Observatoire pour la Mineralogie, l'Eau, les Glaces et l'Activité (OMEGA) instrument on the European Space Agency's Mars Express spacecraft provides new information on Mars' geological and climatic history. Phyllosilicates formed by aqueous alteration very early in the planet's history (the "phyllocian" era) are found in the oldest terrains; sulfates were formed in a second era (the "theiikian" era) in an acidic environment. Beginning about 3.5 billion years ago, the last era (the "siderikian") is dominated by the formation of anhydrous ferric oxides in a slow superficial weathering, without liquid water playing a major role across the planet.
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            Microbial communities in acid mine drainage.

            The dissolution of sulfide minerals such as pyrite (FeS2), arsenopyrite (FeAsS), chalcopyrite (CuFeS2), sphalerite (ZnS), and marcasite (FeS2) yields hot, sulfuric acid-rich solutions that contain high concentrations of toxic metals. In locations where access of oxidants to sulfide mineral surfaces is increased by mining, the resulting acid mine drainage (AMD) may contaminate surrounding ecosystems. Communities of autotrophic and heterotrophic archaea and bacteria catalyze iron and sulfur oxidation, thus may ultimately determine the rate of release of metals and sulfur to the environment. AMD communities contain fewer prokaryotic lineages than many other environments. However, it is notable that at least two archaeal and eight bacterial divisions have representatives able to thrive under the extreme conditions typical of AMD. AMD communities are characterized by a very limited number of distinct species, probably due to the small number of metabolically beneficial reactions available. The metabolisms that underpin these communities include organoheterotrophy and autotrophic iron and sulfur oxidation. Other metabolic activity is based on anaerobic sulfur oxidation and ferric iron reduction. Evidence for physiological synergy in iron, sulfur, and carbon flow in these communities is reviewed. The microbial and geochemical simplicity of these systems makes them ideal targets for quantitative, genomic-based analyses of microbial ecology and evolution and community function.
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              The Opportunity Rover's Athena science investigation at Meridiani Planum, Mars.

              The Mars Exploration Rover Opportunity has investigated the landing site in Eagle crater and the nearby plains within Meridiani Planum. The soils consist of fine-grained basaltic sand and a surface lag of hematite-rich spherules, spherule fragments, and other granules. Wind ripples are common. Underlying the thin soil layer, and exposed within small impact craters and troughs, are flat-lying sedimentary rocks. These rocks are finely laminated, are rich in sulfur, and contain abundant sulfate salts. Small-scale cross-lamination in some locations provides evidence for deposition in flowing liquid water. We interpret the rocks to be a mixture of chemical and siliciclastic sediments formed by episodic inundation by shallow surface water, followed by evaporation, exposure, and desiccation. Hematite-rich spherules are embedded in the rock and eroding from them. We interpret these spherules to be concretions formed by postdepositional diagenesis, again involving liquid water.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                29 April 2015
                2015
                : 10
                : 4
                : e0122869
                Affiliations
                [1 ]Science, Technology, and International Affairs, Georgetown University, Washington, District of Columbia, United States of America
                [2 ]Graduate Program in Biotechnology and Bioengineering, Harvard University Extension, Cambridge, Massachusetts, United States of America
                [3 ]Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, United States of America
                [4 ]Jet Propulsion Laboratory, California Institute of Technology, Pasadena, California, United States of America
                [5 ]Department of Geology and Geography, West Virginia University, Morgantown, West Virginia, United States of America
                Belgian Nuclear Research Centre SCK•CEN, BELGIUM
                Author notes

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

                Conceived and designed the experiments: SSJ. Performed the experiments: SSJ BLE. Analyzed the data: SSJ MGC BLE. Contributed reagents/materials/analysis tools: SSJ MGC BLE KCB. Wrote the paper: SSJ MGC BLE KCB.

                Article
                PONE-D-14-41184
                10.1371/journal.pone.0122869
                4414474
                25923206
                15f5e1dc-dbd1-4c79-9253-e5b514b23763
                Copyright @ 2015

                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
                : 12 September 2014
                : 24 February 2015
                Page count
                Figures: 5, Tables: 2, Pages: 19
                Funding
                This research was supported by a William F. Milton Fund grant to SSJ ( http://www.faculty.harvard.edu/scholarship-and-research/grants-enabling-research/william-f-milton-fund). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                The sequences are publicly available on the NCBI server under project ID PRJNA260488.

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