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      Microbial Activities and Dissolved Organic Matter Dynamics in Oil-Contaminated Surface Seawater from the Deepwater Horizon Oil Spill Site

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          Abstract

          The Deepwater Horizon oil spill triggered a complex cascade of microbial responses that reshaped the dynamics of heterotrophic carbon degradation and the turnover of dissolved organic carbon (DOC) in oil contaminated waters. Our results from 21-day laboratory incubations in rotating glass bottles (roller bottles) demonstrate that microbial dynamics and carbon flux in oil-contaminated surface water sampled near the spill site two weeks after the onset of the blowout were greatly affected by activities of microbes associated with macroscopic oil aggregates. Roller bottles with oil-amended water showed rapid formation of oil aggregates that were similar in size and appearance compared to oil aggregates observed in surface waters near the spill site. Oil aggregates that formed in roller bottles were densely colonized by heterotrophic bacteria, exhibiting high rates of enzymatic activity (lipase hydrolysis) indicative of oil degradation. Ambient waters surrounding aggregates also showed enhanced microbial activities not directly associated with primary oil-degradation (β-glucosidase; peptidase), as well as a twofold increase in DOC. Concurrent changes in fluorescence properties of colored dissolved organic matter (CDOM) suggest an increase in oil-derived, aromatic hydrocarbons in the DOC pool. Thus our data indicate that oil aggregates mediate, by two distinct mechanisms, the transfer of hydrocarbons to the deep sea: a microbially-derived flux of oil-derived DOC from sinking oil aggregates into the ambient water column, and rapid sedimentation of the oil aggregates themselves, serving as vehicles for oily particulate matter as well as oil aggregate-associated microbial communities.

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          Most cited references42

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          In situ settling behavior of marine snow1

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            Marine optical biogeochemistry: the chemistry of ocean color.

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              Microbial extracellular enzymes and the marine carbon cycle.

              Extracellular enzymes initiate microbial remineralization of organic matter by hydrolyzing substrates to sizes sufficiently small to be transported across cell membranes. As much of marine primary productivity is processed by heterotrophic microbes, the substrate specificities of extracellular enzymes, the rates at which they function in seawater and sediments, and factors controlling their production, distribution, and active lifetimes, are central to carbon cycling in marine systems. In this review, these topics are considered from biochemical, microbial/molecular biological, and geochemical perspectives. Our understanding of the capabilities and limitations of heterotrophic microbial communities has been greatly advanced in recent years, in part through genetic and genomic approaches. New methods to measure enzyme activities in the field are needed to keep pace with these advances and to pursue intriguing evidence that patterns of enzyme activities in different environments are linked to differences in microbial community composition that may profoundly affect the marine carbon cycle.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                11 April 2012
                : 7
                : 4
                : e34816
                Affiliations
                [1 ]Department of Marine Sciences, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America
                [2 ]Department of Marine, Earth and Atmospheric Sciences, North Carolina State University, Raleigh, North Carolina, United States of America
                University of California Merced, United States of America
                Author notes

                Conceived and designed the experiments: KZ CA AT. Performed the experiments: KZ LM BR JD-B. Analyzed the data: KZ CO. Wrote the paper: KZ CA AT. Collected seawater on board R/V Pelican: LM.

                Article
                PONE-D-11-19663
                10.1371/journal.pone.0034816
                3324544
                22509359
                c1529428-e636-4422-bbe8-d056356eb921
                Ziervogel 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
                : 6 October 2011
                : 6 March 2012
                Page count
                Pages: 10
                Categories
                Research Article
                Biology
                Biotechnology
                Environmental Biotechnology
                Ecology
                Ecological Environments
                Aquatic Environments
                Microbial Ecology
                Microbiology
                Chemistry
                Environmental Chemistry
                Geochemistry
                Earth Sciences
                Environmental Sciences
                Marine and Aquatic Sciences
                Oceanography
                Biological Oceanography
                Chemical Oceanography
                Marine Ecology

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                Uncategorized

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