Contrasting Effects of Dissolved Organic Matter on Mercury Methylation by Geobacter sulfurreducens PCA and Desulfovibrio desulfuricans ND132

Zhao, Linduo; Chen, Hongmei; Lu, Xia; Lin, Hui; Christensen, Geoff A.; Pierce, Eric M.; Gu, Baohua

doi:10.1021/acs.est.7b02518

Title: Contrasting Effects of Dissolved Organic Matter on Mercury Methylation by Geobacter sulfurreducens PCA and Desulfovibrio desulfuricans ND132

Journal Article · Tue Aug 29 00:00:00 EDT 2017 · Environmental Science and Technology

DOI:https://doi.org/10.1021/acs.est.7b02518· OSTI ID:1377645

^[1]; Chen, Hongmei ^[1]; Lu, Xia ^[1]; Lin, Hui ^[1]; Christensen, Geoff A. ^[2];

^[1];

^[1]

Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States
Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States

Natural dissolved organic matter (DOM) affects mercury (Hg) redox reactions and anaerobic microbial Hg methylation in the environment. Several studies have shown that DOM can enhance Hg methylation, especially under sulfidic conditions, whereas others show that DOM inhibits Hg methylation due to strong Hg-DOM complexation. Here, we investigated and compared the effects of DOM on Hg methylation by an iron-reducing bacterium Geobacter sulfurreducens PCA and a sulfate-reducing bacterium Desulfovibrio desulfuricans ND132 under non-sulfidic conditions. The methylation experiment was performed with washed cells either in the absence or presence of DOM or glutathione, both of which form strong complexes with Hg via thiol-functional groups. DOM was found to greatly inhibit Hg methylation by G. Sulfurreducens PCA but enhance Hg methylation by D. desulfuricans ND132 cells with increasing DOM concentration. Furthermore, these strain-dependent opposing effects of DOM were also observed with glutathione, suggesting that thiols in DOM likely played an essential role in affecting cell Hg uptake and methylation. Additionally, DOM and glutathione decreased Hg sorption by G. sulfurreducens PCA, but not by D. desulfuricans ND132 cells, demonstrating that ND132 has a higher affinity to sorb or take up Hg than the PCA strain. Finally, these observations indicate that DOM effects on Hg methylation are bacterial strain specific, depend on the DOM:Hg ratio or site-specific conditions, and may thus offer new insights into the role of DOM in methylmercury production in the environment.

View Journal Article

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (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:: 1377645

Alternate ID(s):: OSTI ID: 1376646

Journal Information:: Environmental Science and Technology, Journal Name: Environmental Science and Technology Vol. 51 Journal Issue: 18; ISSN 0013-936X

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 67 works

Citation information provided by
Web of Science

References (55)

Development and Validation of Broad-Range Qualitative and Clade-Specific Quantitative Molecular Probes for Assessing Mercury Methylation in the Environment Christensen, Geoff A.; Wymore, Ann M.; King, Andrew J. Applied and Environmental Microbiology, Vol. 82, Issue 19 https://doi.org/10.1128/AEM.01271-16	journal	July 2016
Intracellular Hg(0) Oxidation in Desulfovibrio desulfuricans ND132 Wang, Yuwei; Schaefer, Jeffra K.; Mishra, Bhoopesh Environmental Science & Technology, Vol. 50, Issue 20 https://doi.org/10.1021/acs.est.6b03299	journal	October 2016
Molecular composition of organic matter controls methylmercury formation in boreal lakes Bravo, Andrea G.; Bouchet, Sylvain; Tolu, Julie Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14255	journal	February 2017
Binding Constants of Mercury and Dissolved Organic Matter Determined by a Modified Ion Exchange Technique Dong, Wenming; Bian, Yongrong; Liang, Liyuan Environmental Science & Technology, Vol. 45, Issue 8 https://doi.org/10.1021/es104207g	journal	April 2011
Modeling of the structure-specific kinetics of abiotic, dark reduction of Hg(II) complexed by O/N and S functional groups in humic acids while accounting for time-dependent structural rearrangement Jiang, Tao; Skyllberg, Ulf; Wei, Shiqiang Geochimica et Cosmochimica Acta, Vol. 154 https://doi.org/10.1016/j.gca.2015.01.011	journal	April 2015
Organic Material: The Primary Control on Mercury Methylation and Ambient Methyl Mercury Concentrations in Estuarine Sediments Lambertsson, Lars; Nilsson, Mats Environmental Science & Technology, Vol. 40, Issue 6 https://doi.org/10.1021/es051785h	journal	March 2006
Cysteine Inhibits Mercury Methylation by Geobacter sulfurreducens PCA Mutant Δ omcBESTZ Lin, Hui; Lu, Xia; Liang, Liyuan Environmental Science & Technology Letters, Vol. 2, Issue 5 https://doi.org/10.1021/acs.estlett.5b00068	journal	April 2015
Sulfide Controls on Mercury Speciation and Bioavailability to Methylating Bacteria in Sediment Pore Waters Benoit, Janina M.; Gilmour, Cynthia C.; Mason, Robert P. Environmental Science & Technology, Vol. 33, Issue 6 https://doi.org/10.1021/es9808200	journal	March 1999
Mercury Methylation by Novel Microorganisms from New Environments Gilmour, Cynthia C.; Podar, Mircea; Bullock, Allyson L. Environmental Science & Technology, Vol. 47, Issue 20 https://doi.org/10.1021/es403075t	journal	September 2013
Mercury Reduction and Oxidation by Reduced Natural Organic Matter in Anoxic Environments Zheng, Wang; Liang, Liyuan; Gu, Baohua Environmental Science & Technology, Vol. 46, Issue 1 https://doi.org/10.1021/es203402p	journal	November 2011
Controls on Bacterial Cell Envelope Sulfhydryl Site Concentrations: The Effect of Glucose Concentration During Growth Yu, Qiang; Fein, Jeremy B. Environmental Science & Technology, Vol. 51, Issue 13 https://doi.org/10.1021/acs.est.7b01047	journal	June 2017
Relationship between Extracellular Low-Molecular-Weight Thiols and Mercury Species in Natural Lake Periphytic Biofilms Leclerc, Maxime; Planas, Dolors; Amyot, Marc Environmental Science & Technology, Vol. 49, Issue 13 https://doi.org/10.1021/es505952x	journal	June 2015
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
Complexation of Mercury(II) in Soil Organic Matter: EXAFS Evidence for Linear Two-Coordination with Reduced Sulfur Groups Skyllberg, Ulf; Bloom, Paul R.; Qian, Jin Environmental Science & Technology, Vol. 40, Issue 13 https://doi.org/10.1021/es0600577	journal	July 2006
Biogeochemical factors affecting mercury methylation rate in two contaminated floodplain soils Frohne, T.; Rinklebe, J.; Langer, U. Biogeosciences, Vol. 9, Issue 1 https://doi.org/10.5194/bg-9-493-2012	journal	January 2012
Sulfate-Reducing Bacterium Desulfovibrio desulfuricans ND132 as a Model for Understanding Bacterial Mercury Methylation Gilmour, Cynthia C.; Elias, Dwayne A.; Kucken, Amy M. Applied and Environmental Microbiology, Vol. 77, Issue 12, p. 3938-3951 https://doi.org/10.1128/AEM.02993-10	journal	April 2011
Mercury and Other Heavy Metals Influence Bacterial Community Structure in Contaminated Tennessee Streams Vishnivetskaya, Tatiana A.; Mosher, Jennifer J.; Palumbo, Anthony V. Applied and Environmental Microbiology, Vol. 77, Issue 1 https://doi.org/10.1128/AEM.01715-10	journal	November 2010
Site-Directed Mutagenesis of HgcA and HgcB Reveals Amino Acid Residues Important for Mercury Methylation Smith, Steven D.; Bridou, Romain; Johs, Alexander Applied and Environmental Microbiology, Vol. 81, Issue 9 https://doi.org/10.1128/AEM.00217-15	journal	February 2015
Molecular formulae of marine and terrigenous dissolved organic matter detected by electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry Koch, Boris P.; Witt, Matthias; Engbrodt, Ralph Geochimica et Cosmochimica Acta, Vol. 69, Issue 13 https://doi.org/10.1016/j.gca.2005.02.027	journal	July 2005
Proteomics of Desulfovibrio desulfuricans and X-ray absorption spectroscopy to investigate mercury methylation in the presence of selenium Truong, Hoang-Yen Thi; Chen, Yu-Wei; Saleh, Mazen Metallomics, Vol. 6, Issue 3 https://doi.org/10.1039/c3mt00323j	journal	January 2014
Effect of Dissolved Organic Matter Source and Character on Microbial Hg Methylation in Hg–S–DOM Solutions Graham, Andrew M.; Aiken, George R.; Gilmour, Cynthia C. Environmental Science & Technology, Vol. 47, Issue 11 https://doi.org/10.1021/es400414a	journal	May 2013
The Effect of Natural Organic Matter on Mercury Methylation by Desulfobulbus propionicus 1pr3 Moreau, John W.; Gionfriddo, Caitlin M.; Krabbenhoft, David P. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01389	journal	December 2015
Effect of the Deletion of qmoABC and the Promoter-Distal Gene Encoding a Hypothetical Protein on Sulfate Reduction in Desulfovibrio vulgaris Hildenborough Zane, G. M.; Yen, H. -c. B.; Wall, J. D. Applied and Environmental Microbiology, Vol. 76, Issue 16 https://doi.org/10.1128/AEM.00691-10	journal	June 2010
The Genetic Basis for Bacterial Mercury Methylation Parks, J. M.; Johs, A.; Podar, M. Science, Vol. 339, Issue 6125, p. 1332-1335 https://doi.org/10.1126/science.1230667	journal	February 2013
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
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
Mercury Reduction and Cell-Surface Adsorption by Geobacter sulfurreducens PCA Hu, Haiyan; Lin, Hui; Zheng, Wang Environmental Science & Technology, Vol. 47, Issue 19 https://doi.org/10.1021/es400527m	journal	September 2013
Dissolved Organic Carbon Thresholds Affect Mercury Bioaccumulation in Arctic Lakes French, Todd D.; Houben, Adam J.; Desforges, Jean-Pierre W. Environmental Science & Technology, Vol. 48, Issue 6 https://doi.org/10.1021/es403849d	journal	February 2014
Mercury reduction and complexation by natural organic matter in anoxic environments Gu, B.; Bian, Y.; Miller, C. L. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1008747108	journal	January 2011
Bioaccumulation of mercury in pelagic freshwater food webs Watras, C. J.; Back, R. C.; Halvorsen, S. Science of The Total Environment, Vol. 219, Issue 2-3 https://doi.org/10.1016/S0048-9697(98)00228-9	journal	August 1998
Effects of Cellular Sorption on Mercury Bioavailability and Methylmercury Production by Desulfovibrio desulfuricans ND132 Liu, Yu-Rong; Lu, Xia; Zhao, Linduo Environmental Science & Technology, Vol. 50, Issue 24 https://doi.org/10.1021/acs.est.6b04041	journal	November 2016
Identification of Mercury and Dissolved Organic Matter Complexes Using Ultrahigh Resolution Mass Spectrometry Chen, Hongmei; Johnston, Ryne C.; Mann, Benjamin F. Environmental Science & Technology Letters, Vol. 4, Issue 2 https://doi.org/10.1021/acs.estlett.6b00460	journal	December 2016
Global Proteome Response to Deletion of Genes Related to Mercury Methylation and Dissimilatory Metal Reduction Reveals Changes in Respiratory Metabolism in Geobacter sulfurreducens PCA Qian, Chen; Johs, Alexander; Chen, Hongmei Journal of Proteome Research, Vol. 15, Issue 10 https://doi.org/10.1021/acs.jproteome.6b00263	journal	September 2016
Enhanced availability of mercury bound to dissolved organic matter for methylation in marine sediments Mazrui, Nashaat M.; Jonsson, Sofi; Thota, Sravan Geochimica et Cosmochimica Acta, Vol. 194 https://doi.org/10.1016/j.gca.2016.08.019	journal	December 2016
Mercury Methylation from Unexpected Sources: Molybdate-Inhibited Freshwater Sediments and an Iron-Reducing Bacterium Fleming, E. J.; Mack, E. E.; Green, P. G. Applied and Environmental Microbiology, Vol. 72, Issue 1 https://doi.org/10.1128/AEM.72.1.457-464.2006	journal	January 2006
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
Thiol-Facilitated Cell Export and Desorption of Methylmercury by Anaerobic Bacteria Lin, Hui; Lu, Xia; Liang, Liyuan Environmental Science & Technology Letters, Vol. 2, Issue 10 https://doi.org/10.1021/acs.estlett.5b00209	journal	September 2015
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
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
Influence of Dissolved Organic Matter on the Environmental Fate of Metals, Nanoparticles, and Colloids Aiken, George R.; Hsu-Kim, Heileen; Ryan, Joseph N. Environmental Science & Technology, Vol. 45, Issue 8 https://doi.org/10.1021/es103992s	journal	April 2011
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
Influence of natural dissolved organic carbon on the bioavailability of mercury to a freshwater alga Gorski, P. R.; Armstrong, D. E.; Hurley, J. P. Environmental Pollution, Vol. 154, Issue 1 https://doi.org/10.1016/j.envpol.2007.12.004	journal	July 2008
Anaerobic oxidation of Hg(0) and methylmercury formation by Desulfovibrio desulfuricans ND132 Colombo, Matthew J.; Ha, Juyoung; Reinfelder, John R. Geochimica et Cosmochimica Acta, Vol. 112 https://doi.org/10.1016/j.gca.2013.03.001	journal	July 2013
Methylmercury Production in Estuarine Sediments: Role of Organic Matter Schartup, Amina T.; Mason, Robert P.; Balcom, Prentiss H. Environmental Science & Technology, Vol. 47, Issue 2 https://doi.org/10.1021/es302566w	journal	December 2012
Binding of Mercury(II) to Dissolved Organic Matter: The Role of the Mercury-to-DOM Concentration Ratio Haitzer, Markus; Aiken, George R.; Ryan, Joseph N. Environmental Science & Technology, Vol. 36, Issue 16 https://doi.org/10.1021/es025699i	journal	August 2002
Geochemical Controls on the Production and Distribution of Methylmercury in Near-Shore Marine Sediments Hammerschmidt, Chad R.; Fitzgerald, William F. Environmental Science & Technology, Vol. 38, Issue 5 https://doi.org/10.1021/es034528q	journal	March 2004
Competitive ligand exchange reveals time dependant changes in the reactivity of Hg–dissolved organic matter complexes Miller, Carrie L.; Liang, Liyuan; Gu, Baohua Environmental Chemistry, Vol. 9, Issue 6 https://doi.org/10.1071/EN12096	journal	January 2012
A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater: SPE-DOM from seawater Dittmar, Thorsten; Koch, Boris; Hertkorn, Norbert Limnology and Oceanography: Methods, Vol. 6, Issue 6 https://doi.org/10.4319/lom.2008.6.230	journal	June 2008
Detailed Assessment of the Kinetics of Hg-Cell Association, Hg Methylation, and Methylmercury Degradation in Several Desulfovibrio Species Graham, Andrew M.; Bullock, Allyson L.; Maizel, Andrew C. Applied and Environmental Microbiology, Vol. 78, Issue 20, p. 7337-7346 https://doi.org/10.1128/AEM.01792-12	journal	August 2012
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
Oxidation of Dissolved Elemental Mercury by Thiol Compounds under Anoxic Conditions Zheng, Wang; Lin, Hui; Mann, Benjamin F. Environmental Science & Technology, Vol. 47, Issue 22 https://doi.org/10.1021/es402697u	journal	November 2013
Why Mercury Prefers Soft Ligands Riccardi, Demian; Guo, Hao-Bo; Parks, Jerry M. The Journal of Physical Chemistry Letters, Vol. 4, Issue 14 https://doi.org/10.1021/jz401075b	journal	June 2013
Organic matter and sulfide inhibit methylmercury production in sediments of New York/New Jersey Harbor Hammerschmidt, Chad R.; Fitzgerald, William F.; Balcom, Prentiss H. Marine Chemistry, Vol. 109, Issue 1-2 https://doi.org/10.1016/j.marchem.2008.01.007	journal	February 2008
Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals Lovley, D. R.; Giovannoni, S. J.; White, D. C. Archives of Microbiology, Vol. 159, Issue 4 https://doi.org/10.1007/BF00290916	journal	April 1993
Roles of dissolved organic matter in the speciation of mercury and methylmercury in a contaminated ecosystem in Oak Ridge, Tennessee Dong, Wenming; Liang, Liyuan; Brooks, Scott Environmental Chemistry, Vol. 7, Issue 1 https://doi.org/10.1071/EN09091	journal	January 2010

Similar Records

Enhanced Production of Bioethanol by Fermentation of Autohydrolyzed and C4mimOAc-Treated Sugarcane Bagasse Employing Various Yeast Strains

Journal Article · Tue Aug 01 00:00:00 EDT 2017 · Energies · OSTI ID:1377645

Hashmi, Muzna; Shah, Aamer; Hameed, Abdul; +1 more

Microbial Oxidation of Hg(0) - Its Effect on Hg Stable Isotope Fractionation and Methylmercury Production

Technical Report · Tue Jun 28 00:00:00 EDT 2016 · OSTI ID:1377645

Yee, Nathan; Barkay, Tamar; Reinfelder, John

The sulfate-reducing bacterium Desulfovibrio desulfuricans ND132 as a model for understanding bacterial mercury methylation

Conference · Fri Jan 01 00:00:00 EST 2010 · OSTI ID:1377645

Gilmour, C C; Elias, Dwayne A; Kucken, A M; +3 more

Related Subjects

54 ENVIRONMENTAL SCIENCES

Title: Contrasting Effects of Dissolved Organic Matter on Mercury Methylation by Geobacter sulfurreducens PCA and Desulfovibrio desulfuricans ND132

Citation Formats

References (55)

Similar Records

Related Subjects