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      Mercury and Selenium in Stranded Indo-Pacific Humpback Dolphins and Implications for Their Trophic Transfer in Food Chains

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          Abstract

          As top predators in the Pearl River Estuary (PRE) of China, Indo-Pacific humpback dolphins ( Sousa chinensis) are bioindicators for examining regional trends of environmental contaminants in the PRE. We examined samples from stranded S. chinensis in the PRE, collected since 2004, to study the distribution and fate of total mercury (THg), methylmercury (MeHg) and selenium (Se) in the major tissues, in individuals at different ages and their prey fishes from the PRE. This study also investigated the potential protective effects of Se against the toxicities of accumulated THg. Dolphin livers contained the highest concentrations of THg (32.34±58.98 µg g −1 dw) and Se (15.16±3.66 µg g −1 dw), which were significantly different from those found in kidneys and muscles, whereas the highest residue of MeHg (1.02±1.11 µg g −1 dw) was found in dolphin muscles. Concentrations of both THg and MeHg in the liver, kidney and muscle of dolphins showed a significantly positive correlation with age. The biomagnification factors (BMFs) of inorganic mercury (Hg inorg) in dolphin livers (350×) and MeHg in muscles (18.7×) through the prey fishes were the highest among all three dolphin tissues, whereas the BMFs of Se were much lower in all dolphin tissues. The lower proportion of MeHg in THg and higher Se/THg ratios in tissues were demonstrated. Our studies suggested that S. chinensis might have the potential to detoxify Hg via the demethylation of MeHg and the formation of tiemannite (HgSe) in the liver and kidney. The lower threshold of hepatic THg concentrations for the equimolar accumulation of Se and Hg in S. chinensis suggests that this species has a greater sensitivity to THg concentrations than is found in striped dolphins and Dall’s porpoises.

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          Most cited references25

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          Mercury-selenium compounds and their toxicological significance: toward a molecular understanding of the mercury-selenium antagonism.

          The interaction between mercury (Hg) and selenium (Se) is one of the best known examples of biological antagonism, yet the underlying mechanism remains unclear. This review focuses on the possible pathways leading to the Hg-Se antagonism, with an emphasis on the potential Hg-Se compounds that are responsible for the antagonism at the molecular level (i.e., bis[methylmercuric]selenide, methylmercury selenocysteinate, selenoprotein P-bound HgSe clusters, and the biominerals HgSe(x)S(1-x)). The presence of these compounds in biological systems has been suggested by direct or indirect evidence, and their chemical properties support their potentially key roles in alleviating the toxicity of Hg and Se (at high Hg and Se exposures, respectively) and deficiency of Se (at low Se exposures). Direct analytical evidences are needed, however, to confirm their in vivo presence and metabolic pathways, as well as to identify the roles of other potential Hg-Se compounds. Further studies are also warranted for the determination of thermodynamic properties of these compounds under physiological conditions toward a better understanding of the Hg-Se antagonism in biota, particularly under real world exposure scenarios.
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            Contribution of coexisting sulfate and iron reducing bacteria to methylmercury production in freshwater river sediments.

            We investigated microbial methylmercury (CH(3)Hg) production in sediments from the South River (SR), VA, an ecosystem contaminated with industrial mercury (Hg). Potential Hg methylation rates in samples collected at nine sites were low in late spring and significantly higher in late summer. Demethylation of (14)CH(3)Hg was dominated by (14)CH(4) production in spring, but switched to producing mostly (14)CO(2) in the summer. Fine-grained sediments originating from the erosion of river banks had the highest CH(3)Hg concentrations and were potential hot spots for both methylation and demethylation activities. Sequencing of 16S rRNA genes of cDNA recovered from sediment RNA extracts indicated that at least three groups of sulfate-reducing bacteria (SRB) and one group of iron-reducing bacteria (IRB), potential Hg methylators, were active in SR sediments. SRB were confirmed as a methylating guild by amendment experiments showing significant sulfate stimulation and molybdate inhibition of methylation in SR sediments. The addition of low levels of amorphous iron(III) oxyhydroxide significantly stimulated methylation rates, suggesting a role for IRB in CH(3)Hg synthesis. Overall, our studies suggest that coexisting SRB and IRB populations in river sediments contribute to Hg methylation, possibly by temporally and spatially separated processes.
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              Mercury methylation by the methanogen Methanospirillum hungatei.

              Methylmercury (MeHg), a neurotoxic substance that accumulates in aquatic food chains and poses a risk to human health, is synthesized by anaerobic microorganisms in the environment. To date, mercury (Hg) methylation has been attributed to sulfate- and iron-reducing bacteria (SRB and IRB, respectively). Here we report that a methanogen, Methanospirillum hungatei JF-1, methylated Hg in a sulfide-free medium at comparable rates, but with higher yields, than those observed for some SRB and IRB. Phylogenetic analyses showed that the concatenated orthologs of the Hg methylation proteins HgcA and HgcB from M. hungatei are closely related to those from known SRB and IRB methylators and that they cluster together with proteins from eight other methanogens, suggesting that these methanogens may also methylate Hg. Because all nine methanogens with HgcA and HgcB orthologs belong to the class Methanomicrobia, constituting the late-evolving methanogenic lineage, methanogenic Hg methylation could not be considered an ancient metabolic trait. Our results identify methanogens as a new guild of Hg-methylating microbes with a potentially important role in mineral-poor (sulfate- and iron-limited) anoxic freshwater environments.
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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
                2014
                13 October 2014
                : 9
                : 10
                : e110336
                Affiliations
                [1 ]Guangdong Provincial Key Laboratory of Marine Resources and Coastal Engineering, School of Marine Sciences, Sun Yat-Sen University, Guangzhou, China
                [2 ]Department of Biology, University of Texas at Tyler, Tyler, Texas, United States of America
                [3 ]Urban Environment and Ecology Research Center, South China Institute of Environmental Sciences (SCIES), Ministry of Environmental Protection, Guangzhou, China
                [4 ]South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China
                Oak Ridge National Laboratory, United States of America
                Author notes

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

                Conceived and designed the experiments: YW. Performed the experiments: YS QT HM. Analyzed the data: DG RY YS. Contributed reagents/materials/analysis tools: RY DG. Contributed to the writing of the manuscript: DG YW RY YS. Supervised the research: YW RY LC. Revised the manuscript: DG YR YW.

                Article
                PONE-D-14-11532
                10.1371/journal.pone.0110336
                4195725
                25310100
                5f166e48-56b0-48fd-bf16-7372608d4422
                Copyright @ 2014

                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
                : 25 March 2014
                : 18 September 2014
                Page count
                Pages: 10
                Funding
                This research was supported by the National Natural Science Foundation of China (Grant no. 41276147); a Science and Research Project of the Marine Non-profit Industry (Grant no. 201105011-5); the Ocean Park Conservation Foundation, Hong Kong; the National Key Technology R & D Program (Grant no. 2011BAG07B05-3); and the Sousa chinensis Conservation Action Project from the Administrator of Ocean and Fisheries of Guangdong Province, China. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Marine Biology
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Ecology and Environmental Sciences
                Bioindicators
                Environmental Protection
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

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