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      Metagenomic analysis and metabolite profiling of deep–sea sediments from the Gulf of Mexico following the Deepwater Horizon oil spill

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          Abstract

          Marine subsurface environments such as deep-sea sediments, house abundant and diverse microbial communities that are believed to influence large-scale geochemical processes. These processes include the biotransformation and mineralization of numerous petroleum constituents. Thus, microbial communities in the Gulf of Mexico are thought to be responsible for the intrinsic bioremediation of crude oil released by the Deepwater Horizon (DWH) oil spill. While hydrocarbon contamination is known to enrich for aerobic, oil-degrading bacteria in deep-seawater habitats, relatively little is known about the response of communities in deep-sea sediments, where low oxygen levels may hinder such a response. Here, we examined the hypothesis that increased hydrocarbon exposure results in an altered sediment microbial community structure that reflects the prospects for oil biodegradation under the prevailing conditions. We explore this hypothesis using metagenomic analysis and metabolite profiling of deep-sea sediment samples following the DWH oil spill. The presence of aerobic microbial communities and associated functional genes was consistent among all samples, whereas, a greater number of Deltaproteobacteria and anaerobic functional genes were found in sediments closest to the DWH blowout site. Metabolite profiling also revealed a greater number of putative metabolites in sediments surrounding the blowout zone relative to a background site located 127 km away. The mass spectral analysis of the putative metabolites revealed that alkylsuccinates remained below detection levels, but a homologous series of benzylsuccinates (with carbon chain lengths from 5 to 10) could be detected. Our findings suggest that increased exposure to hydrocarbons enriches for Deltaproteobacteria, which are known to be capable of anaerobic hydrocarbon metabolism. We also provide evidence for an active microbial community metabolizing aromatic hydrocarbons in deep-sea sediments of the Gulf of Mexico.

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          Most cited references33

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          Global distribution of microbial abundance and biomass in subseafloor sediment.

          The global geographic distribution of subseafloor sedimentary microbes and the cause(s) of that distribution are largely unexplored. Here, we show that total microbial cell abundance in subseafloor sediment varies between sites by ca. five orders of magnitude. This variation is strongly correlated with mean sedimentation rate and distance from land. Based on these correlations, we estimate global subseafloor sedimentary microbial abundance to be 2.9⋅10(29) cells [corresponding to 4.1 petagram (Pg) C and ∼0.6% of Earth's total living biomass]. This estimate of subseafloor sedimentary microbial abundance is roughly equal to previous estimates of total microbial abundance in seawater and total microbial abundance in soil. It is much lower than previous estimates of subseafloor sedimentary microbial abundance. In consequence, we estimate Earth's total number of microbes and total living biomass to be, respectively, 50-78% and 10-45% lower than previous estimates.
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            Distributions of microbial activities in deep subseafloor sediments.

            S D'Hondt (2004)
            Diverse microbial communities and numerous energy-yielding activities occur in deeply buried sediments of the eastern Pacific Ocean. Distributions of metabolic activities often deviate from the standard model. Rates of activities, cell concentrations, and populations of cultured bacteria vary consistently from one subseafloor environment to another. Net rates of major activities principally rely on electron acceptors and electron donors from the photosynthetic surface world. At open-ocean sites, nitrate and oxygen are supplied to the deepest sedimentary communities through the underlying basaltic aquifer. In turn, these sedimentary communities may supply dissolved electron donors and nutrients to the underlying crustal biosphere.
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              Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment.

              The subseafloor marine biosphere may be one of the largest reservoirs of microbial biomass on Earth and has recently been the subject of debate in terms of the composition of its microbial inhabitants, particularly on sediments from the Peru Margin. A metagenomic analysis was made by using whole-genome amplification and pyrosequencing of sediments from Ocean Drilling Program Site 1229 on the Peru Margin to further explore the microbial diversity and overall community composition within this environment. A total of 61.9 Mb of genetic material was sequenced from sediments at horizons 1, 16, 32, and 50 m below the seafloor. These depths include sediments from both primarily sulfate-reducing methane-generating regions of the sediment column. Many genes of the annotated genes, including those encoding ribosomal proteins, corresponded to those from the Chloroflexi and Euryarchaeota. However, analysis of the 16S small-subunit ribosomal genes suggests that Crenarchaeota are the abundant microbial member. Quantitative PCR confirms that uncultivated Crenarchaeota are indeed a major microbial group in these subsurface samples. These findings show that the marine subsurface is a distinct microbial habitat and is different from environments studied by metagenomics, especially because of the predominance of uncultivated archaeal groups.
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                Author and article information

                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                15 March 2013
                2013
                : 4
                : 50
                Affiliations
                [1] 1Baruch Marine Field Laboratory, Belle W. Baruch Institute for Marine and Coastal Sciences, University of South Carolina Georgetown, SC, USA
                [2] 2Department of Microbiology and Plant Biology, University of Oklahoma Norman, OK, USA
                [3] 3Institute for Energy and the Environment, University of Oklahoma Norman, OK, USA
                [4] 4School of Chemistry, Newcastle University Newcastle upon Tyne, UK
                [5] 5Department of Civil and Environmental Engineering, University of Tennessee Knoxville, TN, USA
                [6] 6Department of Microbiology, University of Tennessee Knoxville, TN, USA
                [7] 7 Department of Earth and Planetary Sciences, University of Tennessee Knoxville, TN, USA
                [8] 8Ecology Department, Lawrence Berkeley National Laboratory Berkeley, CA, USA
                Author notes

                Edited by: Rachel Narehood Austin, Bates College, USA

                Reviewed by: John Senko, The University of Akron, USA; John W. Moreau, University of Melbourne, Australia

                *Correspondence: Pamela J. Morris, Baruch Marine Field Laboratory, Belle W. Baruch Institute for Marine and Coastal Sciences, University of South Carolina, PO BOX 1630, Georgetown, SC 29442, USA. e-mail: pjmorris@ 123456belle.baruch.sc.edu

                †Present address: Nikole E. Kimes, Evolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, San Juan, Alicante, Spain.

                This article was submitted to Frontiers in Microbiological Chemistry, a specialty of Frontiers in Microbiology.

                Article
                10.3389/fmicb.2013.00050
                3598227
                23508965
                1735a521-460a-493e-b290-324c33b6cb14
                Copyright © Kimes, Callaghan, Aktas, Smith, Sunner, Golding, Drozdowska, Hazen, Suflita and Morris.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                History
                : 17 December 2012
                : 21 February 2013
                Page count
                Figures: 10, Tables: 2, Equations: 0, References: 61, Pages: 17, Words: 0
                Categories
                Microbiology
                Original Research Article

                Microbiology & Virology
                deepwater horizon,metabolomics,metagenomics,oil-degradation
                Microbiology & Virology
                deepwater horizon, metabolomics, metagenomics, oil-degradation

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