Warming increases methylmercury production in an Arctic soil

Yang, Ziming; Fang, Wei; Lu, Xia; Sheng, Guo-Ping; Graham, David E.; Liang, Liyuan; Wullschleger, Stan D.; Gu, Baohua

doi:10.1016/j.envpol.2016.04.069

Title: Warming increases methylmercury production in an Arctic soil

Journal Article · Fri Apr 29 00:00:00 EDT 2016 · Environmental Pollution

DOI:https://doi.org/10.1016/j.envpol.2016.04.069· OSTI ID:1319169

Yang, Ziming ^[1]; Fang, Wei ^[2]; Lu, Xia ^[1]; Sheng, Guo-Ping ^[3]; Graham, David E. ^[4]; Liang, Liyuan ^[5]; Wullschleger, Stan D. ^[6];

^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division; Univ. of Science and Technology of China, Hefei (China). CAS Key Lab. for Urban Pollutant Conversion
Univ. of Science and Technology of China, Hefei (China). CAS Key Lab. for Urban Pollutant Conversion
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division and Biology and Soft Matter Division
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Environmental Sciences Division and Climate Change Science Inst.

The rapid temperature rise in Arctic permafrost concerns not only the degradation of stored soil organic carbon (SOC) and climate feedback, but also the production and bioaccumulation of methylmercury (MeHg) that may endanger humans, as well as wildlife in terrestrial, aquatic, and marine ecosystems. Decomposition of SOC provides an energy source for microbial methylation, although little is known how rapid permafrost thaw affects Hg methylation and how SOC degradation is coupled to MeHg biosynthesis. We describe rates of MeHg production in Arctic soils from an 8-month warming microcosm experiment under anoxic conditions. MeHg production increased >10 fold in both organic- and the mineral-rich soil layers at a warmer temperature (8 C) compared to a sub-zero temperature ( 2 C). MeHg production was positively correlated to methane and ferrous ion concentrations, suggesting that Hg methylation is coupled with methanogenesis and iron reduction. Labile SOC, such as reducing sugars and alcohol, were particularly effective in fueling the initial rapid biosynthesis of MeHg. In freshly amended Hg we found that there was more bioavailable than existing Hg in the mineral soil. Finally, the data indicate that climate warming and permafrost thaw could greatly enhance MeHg production, thereby impacting Arctic aquatic and marine ecosystems through biomagnification in the food web.

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Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1319169

Alternate ID(s):: OSTI ID: 1341459

Journal Information:: Environmental Pollution, Vol. 214, Issue C; ISSN 0269-7491

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 38 works

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References (41)

Some like it cold: microbial transformations of mercury in polar regions Barkay, Tamar; Kroer, Niels; Poulain, Alexandre J. Polar Research, Vol. 30, Issue 1 https://doi.org/10.3402/polar.v30i0.15469	journal	January 2011
Artifact formation of methyl mercury during aqueous distillation and alternative techniques for the extraction of methyl mercury from environmental samples Bloom, N. S.; Colman, John A.; Barber, Lee Fresenius' Journal of Analytical Chemistry, Vol. 358, Issue 3 https://doi.org/10.1007/s002160050432	journal	June 1997
Dissolved Organic Matter Kinetically Controls Mercury Bioavailability to Bacteria Chiasson-Gould, Sophie A.; Blais, Jules M.; Poulain, Alexandre J. Environmental Science & Technology, Vol. 48, Issue 6 https://doi.org/10.1021/es4038484	journal	February 2014
Over three millennia of mercury pollution in the Peruvian Andes Cooke, C. A.; Balcom, P. H.; Biester, H. Proceedings of the National Academy of Sciences, Vol. 106, Issue 22 https://doi.org/10.1073/pnas.0900517106	journal	May 2009
Anthropogenic contributions to mercury levels in present-day Arctic animals—A review Dietz, Rune; Outridge, Peter M.; Hobson, Keith A. Science of The Total Environment, Vol. 407, Issue 24 https://doi.org/10.1016/j.scitotenv.2009.08.036	journal	December 2009
Dissolved Organic Matter Enhances Microbial Mercury Methylation Under Sulfidic Conditions Graham, Andrew M.; Aiken, George R.; Gilmour, Cynthia C. Environmental Science & Technology, Vol. 46, Issue 5 https://doi.org/10.1021/es203658f	journal	February 2012
Mercury deposition and methylmercury formation in Narraguinnep Reservoir, southwestern Colorado, USA Gray, John E.; Hines, Mark E.; Goldstein, Harland L. Applied Geochemistry, Vol. 50 https://doi.org/10.1016/j.apgeochem.2014.09.001	journal	November 2014
Methanogens: Principal Methylators of Mercury in Lake Periphyton Hamelin, Stéphanie; Amyot, Marc; Barkay, Tamar Environmental Science & Technology, Vol. 45, Issue 18 https://doi.org/10.1021/es2010072	journal	September 2011
Mercury methylation and demethylation by periphyton biofilms and their host in a fluvial wetland of the St. Lawrence River (QC, Canada) Hamelin, Stéphanie; Planas, Dolors; Amyot, Marc Science of The Total Environment, Vol. 512-513 https://doi.org/10.1016/j.scitotenv.2015.01.040	journal	April 2015
Whole-ecosystem study shows rapid fish-mercury response to changes in mercury deposition Harris, R. C.; Rudd, J. W. M.; Amyot, M. Proceedings of the National Academy of Sciences, Vol. 104, Issue 42 https://doi.org/10.1073/pnas.0704186104	journal	September 2007
Pathways of anaerobic organic matter decomposition in tundra soils from Barrow, Alaska: BIOGEOCHEMISTRY OF ANOXIC ARCTIC TUNDRA Herndon, Elizabeth M.; Mann, Benjamin F.; Roy Chowdhury, Taniya Journal of Geophysical Research: Biogeosciences, Vol. 120, Issue 11 https://doi.org/10.1002/2015JG003147	journal	November 2015
Geochemical drivers of organic matter decomposition in arctic tundra soils Herndon, Elizabeth M.; Yang, Ziming; Bargar, John Biogeochemistry, Vol. 126, Issue 3 https://doi.org/10.1007/s10533-015-0165-5	journal	December 2015
Constants of mercury methylation and demethylation rates in sediments and comparison of tracer and ambient mercury availability Hintelmann, Holger; Keppel-Jones, Katherine; Evans, R. Douglas Environmental Toxicology and Chemistry, Vol. 19, Issue 9 https://doi.org/10.1002/etc.5620190909	journal	September 2000
Oxidation and methylation of dissolved elemental mercury by anaerobic bacteria Hu, Haiyan; Lin, Hui; Zheng, Wang Nature Geoscience, Vol. 6, Issue 9 https://doi.org/10.1038/ngeo1894	journal	August 2013
Differentiated availability of geochemical mercury pools controls methylmercury levels in estuarine sediment and biota Jonsson, Sofi; Skyllberg, Ulf; Nilsson, Mats B. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5624	journal	August 2014
Mercury Methylation by Dissimilatory Iron-Reducing Bacteria Kerin, E. J.; Gilmour, C. C.; Roden, E. Applied and Environmental Microbiology, Vol. 72, Issue 12, p. 7919-7921 https://doi.org/10.1128/AEM.01602-06	journal	October 2006
Coupling mercury methylation rates to sulfate reduction rates in marine sediments King, Jeffrey K.; Saunders, F. Michael; Lee, Richard F. Environmental Toxicology and Chemistry, Vol. 18, Issue 7 https://doi.org/10.1002/etc.5620180704	journal	July 1999
Mercury in Arctic marine ecosystems: Sources, pathways and exposure Kirk, Jane L.; Lehnherr, Igor; Andersson, Maria Environmental Research, Vol. 119 https://doi.org/10.1016/j.envres.2012.08.012	journal	November 2012
Methylmercury Cycling in High Arctic Wetland Ponds: Sources and Sinks Lehnherr, Igor; St. Louis, Vincent L.; Emmerton, Craig A. Environmental Science & Technology, Vol. 46, Issue 19 https://doi.org/10.1021/es300576p	journal	July 2012
Methylation of inorganic mercury in polar marine waters Lehnherr, Igor; St. Louis, Vincent L.; Hintelmann, Holger Nature Geoscience, Vol. 4, Issue 5 https://doi.org/10.1038/ngeo1134	journal	April 2011
Coupled Mercury–Cell Sorption, Reduction, and Oxidation on Methylmercury Production by Geobacter sulfurreducens PCA Lin, Hui; Morrell-Falvey, Jennifer L.; Rao, Balaji Environmental Science & Technology, Vol. 48, Issue 20 https://doi.org/10.1021/es502537a	journal	October 2014
Methylmercury Production in high Arctic Wetlands Loseto, Lisa L.; Siciliano, Steven D.; Lean, David R. S. Environmental Toxicology and Chemistry, Vol. 23, Issue 1 https://doi.org/10.1897/02-644	journal	January 2004
Anaerobic Mercury Methylation and Demethylation by Geobacter bemidjiensis Bem Lu, Xia; Liu, Yurong; Johs, Alexander Environmental Science & Technology, Vol. 50, Issue 8 https://doi.org/10.1021/acs.est.6b00401	journal	April 2016
Climate Change, Risks and Contaminants: A Perspective from Studying the Arctic Macdonald, Robie W. Human and Ecological Risk Assessment: An International Journal, Vol. 11, Issue 6 https://doi.org/10.1080/10807030500346482	journal	December 2005
High Methylmercury in Arctic and Subarctic Ponds is Related to Nutrient Levels in the Warming Eastern Canadian Arctic MacMillan, Gwyneth A.; Girard, Catherine; Chételat, John Environmental Science & Technology, Vol. 49, Issue 13 https://doi.org/10.1021/acs.est.5b00763	journal	June 2015
Methyl mercury production and loss in Arctic soil Oiffer, Lindsay; Siciliano, Steven D. Science of The Total Environment, Vol. 407, Issue 5 https://doi.org/10.1016/j.scitotenv.2008.10.025	journal	February 2009
Bioaccumulation of newly deposited mercury by fish and invertebrates: an enclosure study using stable mercury isotopes Paterson, Michael J.; Blanchfield, Paul J.; Podemski, Cheryl Canadian Journal of Fisheries and Aquatic Sciences, Vol. 63, Issue 10 https://doi.org/10.1139/f06-118	journal	October 2006
Global prevalence and distribution of genes and microorganisms involved in mercury methylation Podar, Mircea; Gilmour, Cynthia C.; Brandt, Craig C. Science Advances, Vol. 1, Issue 9 https://doi.org/10.1126/sciadv.1500675	journal	October 2015
Stoichiometry and temperature sensitivity of methanogenesis and CO ₂ production from saturated polygonal tundra in Barrow, Alaska Roy Chowdhury, Taniya; Herndon, Elizabeth M.; Phelps, Tommy J. Global Change Biology, Vol. 21, Issue 2 https://doi.org/10.1111/gcb.12762	journal	November 2014
Climate driven release of carbon and mercury from permafrost mires increases mercury loading to sub-arctic lakes Rydberg, Johan; Klaminder, Jonatan; Rosén, Peter Science of The Total Environment, Vol. 408, Issue 20 https://doi.org/10.1016/j.scitotenv.2010.06.056	journal	September 2010
Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria Schaefer, J. K.; Rocks, S. S.; Zheng, W. Proceedings of the National Academy of Sciences, Vol. 108, Issue 21 https://doi.org/10.1073/pnas.1105781108	journal	May 2011
Freshwater discharges drive high levels of methylmercury in Arctic marine biota Schartup, Amina T.; Balcom, Prentiss H.; Soerensen, Anne L. Proceedings of the National Academy of Sciences, Vol. 112, Issue 38 https://doi.org/10.1073/pnas.1505541112	journal	September 2015
Contrasting Effects of Marine and Terrestrially Derived Dissolved Organic Matter on Mercury Speciation and Bioavailability in Seawater Schartup, Amina T.; Ndu, Udonna; Balcom, Prentiss H. Environmental Science & Technology, Vol. 49, Issue 10 https://doi.org/10.1021/es506274x	journal	May 2015
Climate change and the permafrost carbon feedback Schuur, E. A. G.; McGuire, A. D.; Schädel, C. Nature, Vol. 520, Issue 7546 https://doi.org/10.1038/nature14338	journal	April 2015
A mass budget for mercury and methylmercury in the Arctic Ocean: ARCTIC OCEAN HG AND MEHG MASS BUDGET Soerensen, Anne L.; Jacob, Daniel J.; Schartup, Amina T. Global Biogeochemical Cycles, Vol. 30, Issue 4 https://doi.org/10.1002/2015GB005280	journal	April 2016
Mercury in flux Sonke, Jeroen E.; Heimbürger, Lars-Eric Nature Geoscience, Vol. 5, Issue 7 https://doi.org/10.1038/ngeo1508	journal	June 2012
Temperature and the Sulfur Cycle Control Monomethylmercury Cycling in High Arctic Coastal Marine Sediments from Allen Bay, Nunavut, Canada St. Pierre, K. A.; Chétélat, J.; Yumvihoze, E. Environmental Science & Technology, Vol. 48, Issue 5 https://doi.org/10.1021/es405253g	journal	February 2014
How does climate change influence arctic mercury? Stern, Gary A.; Macdonald, Robie W.; Outridge, Peter M. Science of The Total Environment, Vol. 414 https://doi.org/10.1016/j.scitotenv.2011.10.039	journal	January 2012
Soil organic carbon pools in the northern circumpolar permafrost region: SOIL ORGANIC CARBON POOLS Tarnocai, C.; Canadell, J. G.; Schuur, E. A. G. Global Biogeochemical Cycles, Vol. 23, Issue 2 https://doi.org/10.1029/2008GB003327	journal	June 2009
Microbial Mercury Transformation in Anoxic Freshwater Sediments under Iron-Reducing and Other Electron-Accepting Conditions Warner, Kimberly A.; Roden, Eric E.; Bonzongo, Jean-Claude Environmental Science & Technology, Vol. 37, Issue 10 https://doi.org/10.1021/es0262939	journal	May 2003
Effects of warming on the degradation and production of low-molecular-weight labile organic carbon in an Arctic tundra soil Yang, Ziming; Wullschleger, Stan D.; Liang, Liyuan Soil Biology and Biochemistry, Vol. 95 https://doi.org/10.1016/j.soilbio.2015.12.022	journal	April 2016

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54 ENVIRONMENTAL SCIENCES
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Title: Warming increases methylmercury production in an Arctic soil

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