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      The life sulfuric: microbial ecology of sulfur cycling in marine sediments

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          Summary

          Almost the entire seafloor is covered with sediments that can be more than 10 000 m thick and represent a vast microbial ecosystem that is a major component of Earth's element and energy cycles. Notably, a significant proportion of microbial life in marine sediments can exploit energy conserved during transformations of sulfur compounds among different redox states. Sulfur cycling, which is primarily driven by sulfate reduction, is tightly interwoven with other important element cycles (carbon, nitrogen, iron, manganese) and therefore has profound implications for both cellular‐ and ecosystem‐level processes. Sulfur‐transforming microorganisms have evolved diverse genetic, metabolic, and in some cases, peculiar phenotypic features to fill an array of ecological niches in marine sediments. Here, we review recent and selected findings on the microbial guilds that are involved in the transformation of different sulfur compounds in marine sediments and emphasise how these are interlinked and have a major influence on ecology and biogeochemistry in the seafloor. Extraordinary discoveries have increased our knowledge on microbial sulfur cycling, mainly in sulfate‐rich surface sediments, yet many questions remain regarding how sulfur redox processes may sustain the deep‐subsurface biosphere and the impact of organic sulfur compounds on the marine sulfur cycle.

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          Most cited references169

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          Burial of organic carbon and pyrite sulfur in the modern ocean; its geochemical and environmental significance

          R. Berner (1982)
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            Single cell activity reveals direct electron transfer in methanotrophic consortia.

            Multicellular assemblages of microorganisms are ubiquitous in nature, and the proximity afforded by aggregation is thought to permit intercellular metabolic coupling that can accommodate otherwise unfavourable reactions. Consortia of methane-oxidizing archaea and sulphate-reducing bacteria are a well-known environmental example of microbial co-aggregation; however, the coupling mechanisms between these paired organisms is not well understood, despite the attention given them because of the global significance of anaerobic methane oxidation. Here we examined the influence of interspecies spatial positioning as it relates to biosynthetic activity within structurally diverse uncultured methane-oxidizing consortia by measuring stable isotope incorporation for individual archaeal and bacterial cells to constrain their potential metabolic interactions. In contrast to conventional models of syntrophy based on the passage of molecular intermediates, cellular activities were found to be independent of both species intermixing and distance between syntrophic partners within consortia. A generalized model of electric conductivity between co-associated archaea and bacteria best fit the empirical data. Combined with the detection of large multi-haem cytochromes in the genomes of methanotrophic archaea and the demonstration of redox-dependent staining of the matrix between cells in consortia, these results provide evidence for syntrophic coupling through direct electron transfer.
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              A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast.

              Nitrogen cycling is normally thought to dominate the biogeochemistry and microbial ecology of oxygen-minimum zones in marine environments. Through a combination of molecular techniques and process rate measurements, we showed that both sulfate reduction and sulfide oxidation contribute to energy flux and elemental cycling in oxygen-free waters off the coast of northern Chile. These processes may have been overlooked because in nature, the sulfide produced by sulfate reduction immediately oxidizes back to sulfate. This cryptic sulfur cycle is linked to anammox and other nitrogen cycling processes, suggesting that it may influence biogeochemical cycling in the global ocean.
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                Author and article information

                Contributors
                loy@microbial-ecology.net
                Journal
                Environ Microbiol Rep
                Environ Microbiol Rep
                10.1111/(ISSN)1758-2229
                EMI4
                Environmental Microbiology Reports
                John Wiley and Sons Inc. (Hoboken )
                1758-2229
                05 May 2017
                August 2017
                : 9
                : 4 ( doiID: 10.1111/emi4.2017.9.issue-4 )
                : 323-344
                Affiliations
                [ 1 ] Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, Research Network “Chemistry meets Microbiology” University of Vienna Althanstrasse 14 Vienna A‐1090 Austria
                [ 2 ] Austrian Polar Research Institute Vienna Austria
                Author notes
                [*] [* ]For correspondence. E‐mail loy@ 123456microbial-ecology.net ; Tel. +43 1 4277 76605; Fax +43 1 4277 876605.
                [†]

                All authors contributed equally to this review.

                Author information
                http://orcid.org/0000-0001-8923-5882
                Article
                EMI412538
                10.1111/1758-2229.12538
                5573963
                28419734
                2415fde3-cade-4e22-a4be-53cc1f0dd938
                © 2017 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Figures: 2, Tables: 1, Pages: 22, Words: 14489
                Funding
                Funded by: Austrian Science Fund
                Award ID: P25111‐B22
                Award ID: P29426‐B22
                Categories
                Minireview
                Minireviews
                Custom metadata
                2.0
                emi412538
                August 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.1.8 mode:remove_FC converted:29.08.2017

                Microbiology & Virology
                Microbiology & Virology

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