Synergistic Effects of a Chalkophore, Methanobactin, on Microbial Methylation of Mercury

Yin, Xixiang; Wang, Lihong; Zhang, Lijie; Chen, Hongmei; Liang, Xujun; Lu, Xia; DiSpirito, Alan; Semrau, Jeremy D.; Gu, Baohua

doi:10.1128/AEM.00122-20

Title: Synergistic Effects of a Chalkophore, Methanobactin, on Microbial Methylation of Mercury

Journal Article · Tue May 19 00:00:00 EDT 2020 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/AEM.00122-20· OSTI ID:1615790

Yin, Xixiang ^[1]; Wang, Lihong ^[2];

^[3];

^[4]; Liang, Xujun ^[5];

^[3]; DiSpirito, Alan ^[6]; Semrau, Jeremy D. ^[7];

^[5]

Jinan Research Academy of Environmental Sciences, Jinan (China); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Qilu Univ. of Technology, Jinan (China)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Old Dominion Univ., Norfolk, VA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
Iowa State Univ., Ames, IA (United States)
Univ. of Michigan, Ann Arbor, MI (United States)

Microbial production of the neurotoxin methylmercury (MeHg) is a significant health and environmental concern, as it can bioaccumulate and biomagnify in the food web. A chalkophore or a copper-binding compound, termed methanobactin (MB), has been shown to form strong complexes with mercury [as Hg(II)] and also enables some methanotrophs to degrade MeHg. It is unknown, however, if Hg(II) binding with MB can also impede Hg(II) methylation by other microbes. Contrary to expectations, MB produced by the methanotrophMethylosinus trichosporiumOB3b (OB3b-MB) enhanced the rate and efficiency of Hg(II) methylation more than that observed with thiol compounds (such as cysteine) by the mercury-methylating bacteriaDesulfovibrio desulfuricansND132 andGeobacter sulfurreducensPCA. Compared to no-MB controls, OB3b-MB decreased the rates of Hg(II) sorption and internalization, but increased methylation by 5- to 7-fold, suggesting that Hg(II) complexation with OB3b-MB facilitated exchange and internal transfer of Hg(II) to the HgcAB proteins required for methylation. Conversely, addition of excess amounts of OB3b-MB or a different form of MB fromMethylocystisstrain SB2 (SB2-MB) inhibited Hg(II) methylation, likely due to greater binding of Hg(II). Collectively, our results underscore the complex roles of microbial exogenous metal-scavenging compounds in controlling net production and bioaccumulation of MeHg in the environment. Some anaerobic microorganisms convert inorganic mercury (Hg) into the neurotoxin methylmercury, which can bioaccumulate and biomagnify in the food web. While the genetic basis of microbial mercury methylation is known, factors that control net methylmercury production in the environment are still poorly understood. Here, it is shown that mercury methylation can be substantially enhanced by one form of an exogenous copper-binding compound (methanobactin) produced by some methanotrophs, but not by another. This novel finding illustrates that complex interactions exist between microbes and that these interactions can potentially affect the net production of methylmercuryin situ.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Michigan, Ann Arbor, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Natural Science Foundation of China (NSFC)

Grant/Contract Number:: AC05-00OR22725; SC0018059; 1724430 1724744; 41671485; ZR2017MD008

OSTI ID:: 1615790

Alternate ID(s):: OSTI ID: 1691489

Journal Information:: Applied and Environmental Microbiology, Vol. 86, Issue 11; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 8 works

Citation information provided by
Web of Science

References (46)

Microbial Biosynthesis of Thiol Compounds: Implications for Speciation, Cellular Uptake, and Methylation of Hg(II) Adediran, Gbotemi A.; Liem-Nguyen, Van; Song, Yu Environmental Science & Technology, Vol. 53, Issue 14 https://doi.org/10.1021/acs.est.9b01502	journal	June 2019
Methanotrophs and copper Semrau, Jeremy D.; DiSpirito, Alan A.; Yoon, Sukhwan FEMS Microbiology Reviews, Vol. 34, Issue 4 https://doi.org/10.1111/j.1574-6976.2010.00212.x	journal	July 2010
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
Methanobactin and MmoD work in concert to act as the ‘copper-switch’ in methanotrophs: Copper-switch in methanotrophy Semrau, Jeremy D.; Jagadevan, Sheeja; DiSpirito, Alan A. Environmental Microbiology https://doi.org/10.1111/1462-2920.12150	journal	May 2013
Human Exposure To Methylmercury through Rice Intake in Mercury Mining Areas, Guizhou Province, China Feng, Xinbin; Li, Ping; Qiu, Guangle Environmental Science & Technology, Vol. 42, Issue 1 https://doi.org/10.1021/es071948x	journal	January 2008
Predicting the Bioavailability of Metals and Metal Complexes: Critical Review of the Biotic Ligand Model Slaveykova, Vera I.; Wilkinson, Kevin J. Environmental Chemistry, Vol. 2, Issue 1 https://doi.org/10.1071/EN04076	journal	January 2005
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
Sulfate stimulation of mercury methylation in freshwater sediments Gilmour, Cynthia C.; Henry, Elizabeth A.; Mitchell, Ralph Environmental Science & Technology, Vol. 26, Issue 11 https://doi.org/10.1021/es00035a029	journal	November 1992
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
Methanobactin and the Link between Copper and Bacterial Methane Oxidation DiSpirito, Alan A.; Semrau, Jeremy D.; Murrell, J. Colin Microbiology and Molecular Biology Reviews, Vol. 80, Issue 2 https://doi.org/10.1128/MMBR.00058-15	journal	March 2016
Methane-oxidizing archaea, aerobic methanotrophs and nitrifiers coexist with methane as the sole carbon source Costa, R. B.; Okada, D. Y.; Delforno, T. P. International Biodeterioration & Biodegradation, Vol. 138 https://doi.org/10.1016/j.ibiod.2019.01.005	journal	March 2019
Mercury Sorption and Desorption on Organo-Mineral Particulates as a Source for Microbial Methylation Zhang, Lijie; Wu, Shan; Zhao, Linduo Environmental Science & Technology, Vol. 53, Issue 5 https://doi.org/10.1021/acs.est.8b06020	journal	January 2019
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
Advanced biotic ligand models: Using surface complexation modeling to quantify metal bioavailability to bacteria in geologic systems Fein, Jeremy B. Chemical Geology, Vol. 464 https://doi.org/10.1016/j.chemgeo.2016.10.001	journal	August 2017
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 bioaccumulation increases with latitude in a coastal marine fish (Atlantic silverside, Menidia menidia ) Baumann, Zofia; Mason, Robert P.; Conover, David O. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 74, Issue 7 https://doi.org/10.1139/cjfas-2016-0396	journal	July 2017
Mercury Uptake by Desulfovibrio desulfuricans ND132: Passive or Active? An, Jing; Zhang, Lijie; Lu, Xia Environmental Science & Technology, Vol. 53, Issue 11 https://doi.org/10.1021/acs.est.9b00047	journal	May 2019
Spectroscopic and Microscopic Evidence of Biomediated HgS Species Formation from Hg(II)–Cysteine Complexes: Implications for Hg(II) Bioavailability Thomas, Sara A.; Rodby, Kara E.; Roth, Eric W. Environmental Science & Technology, Vol. 52, Issue 17 https://doi.org/10.1021/acs.est.8b01305	journal	August 2018
Stepwise Reduction Approach Reveals Mercury Competitive Binding and Exchange Reactions within Natural Organic Matter and Mixed Organic Ligands Liang, Xujun; Lu, Xia; Zhao, Jiating Environmental Science & Technology, Vol. 53, Issue 18 https://doi.org/10.1021/acs.est.9b02586	journal	August 2019
Diversity and Habitat Preferences of Cultivated and Uncultivated Aerobic Methanotrophic Bacteria Evaluated Based on pmoA as Molecular Marker Knief, Claudia Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01346	journal	December 2015
Highly efficient methane biocatalysis revealed in a methanotrophic bacterium Kalyuzhnaya, M. G.; Yang, S.; Rozova, O. N. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3785	journal	December 2013
Mercury Adsorption on Minerals and Its Effect on Microbial Methylation Zhao, Linduo; Li, Yunzi; Zhang, Lijie ACS Earth and Space Chemistry, Vol. 3, Issue 7 https://doi.org/10.1021/acsearthspacechem.9b00039	journal	May 2019
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
Nanomolar Copper Enhances Mercury Methylation by Desulfovibrio desulfuricans ND132 Lu, Xia; Johs, Alexander; Zhao, Linduo Environmental Science & Technology Letters, Vol. 5, Issue 6 https://doi.org/10.1021/acs.estlett.8b00232	journal	May 2018
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
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
Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia : Perspectives on methanotrophic Op den Camp, Huub J. M.; Islam, Tajul; Stott, Matthew B. Environmental Microbiology Reports, Vol. 1, Issue 5 https://doi.org/10.1111/j.1758-2229.2009.00022.x	journal	March 2009
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
A TonB-Dependent Transporter Is Responsible for Methanobactin Uptake by Methylosinus trichosporium OB3b Gu, Wenyu; Farhan Ul Haque, Muhammad; Baral, Bipin S. Applied and Environmental Microbiology, Vol. 82, Issue 6 https://doi.org/10.1128/AEM.03884-15	journal	January 2016
Methylmercury uptake and degradation by methanotrophs Lu, Xia; Gu, Wenyu; Zhao, Linduo Science Advances, Vol. 3, Issue 5 https://doi.org/10.1126/sciadv.1700041	journal	May 2017
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
Mercury binding by methanobactin from Methylocystis strain SB2 Baral, Bipin S.; Bandow, Nathan L.; Vorobev, Alexy Journal of Inorganic Biochemistry, Vol. 141 https://doi.org/10.1016/j.jinorgbio.2014.09.004	journal	December 2014
Contrasting Effects of Dissolved Organic Matter on Mercury Methylation by Geobacter sulfurreducens PCA and Desulfovibrio desulfuricans ND132 Zhao, Linduo; Chen, Hongmei; Lu, Xia Environmental Science & Technology, Vol. 51, Issue 18 https://doi.org/10.1021/acs.est.7b02518	journal	August 2017
Bacterial mercury resistance from atoms to ecosystems Barkay, Tamar; Miller, Susan M.; Summers, Anne O. FEMS Microbiology Reviews, Vol. 27, Issue 2-3 https://doi.org/10.1016/S0168-6445(03)00046-9	journal	June 2003
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
Methanobactin from Methylosinus trichosporium OB3b inhibits N2O reduction in denitrifiers Chang, Jin; Gu, Wenyu; Park, Doyoung The ISME Journal, Vol. 12, Issue 8 https://doi.org/10.1038/s41396-017-0022-8	journal	January 2018
Bioaccumulation of mercury and methylmercury Mason, R. P.; Reinfelder, J. R.; Morel, F. M. M. Water, Air, & Soil Pollution, Vol. 80, Issue 1-4 https://doi.org/10.1007/BF01189744	journal	February 1995
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
High resolution depth distribution of Bacteria, Archaea, methanotrophs, and methanogens in the bulk and rhizosphere soils of a flooded rice paddy Lee, Hyo Jung; Jeong, Sang Eun; Kim, Pil Joo Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00639	journal	June 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
Spectral and thermodynamic properties of Ag(I), Au(III), Cd(II), Co(II), Fe(III), Hg(II), Mn(II), Ni(II), Pb(II), U(IV), and Zn(II) binding by methanobactin from Methylosinus trichosporium OB3b Choi, Dong W.; Do, Young S.; Zea, Corbin J. Journal of Inorganic Biochemistry, Vol. 100, Issue 12, p. 2150-2161 https://doi.org/10.1016/j.jinorgbio.2006.08.017	journal	December 2006
Detoxification of Mercury by Methanobactin from Methylosinus trichosporium OB3b Vorobev, Alexey; Jagadevan, Sheeja; Baral, Bipin S. Applied and Environmental Microbiology, Vol. 79, Issue 19 https://doi.org/10.1128/AEM.01673-13	journal	July 2013

Similar Records

Methanotrophic-Mediated Methylmercury Transformation: Characterization of Products, Mechanism, and Environmental Significance (Final Technical Report)

Technical Report · Mon Nov 02 00:00:00 EST 2020 · OSTI ID:1615790

Semrau, Jeremy D.; Gu, Baohua

Kinetics of Enzymatic Mercury Methylation at Nanomolar Concentrations Catalyzed by HgcAB

Journal Article · Fri Apr 26 00:00:00 EDT 2019 · Applied and Environmental Microbiology · OSTI ID:1615790

Date, Swapneeta S.; Parks, Jerry M.; Rush, Katherine W.; +3 more

Carbon Amendments Alter Microbial Community Structure and Net Mercury Methylation Potential in Sediments

Journal Article · Thu Feb 01 00:00:00 EST 2018 · Applied and Environmental Microbiology · OSTI ID:1615790

Christensen, Geoff A.; Somenahally, Anil C.; Moberly, James G.; +11 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
54 ENVIRONMENTAL SCIENCES
methanobactin
methylmercury

Title: Synergistic Effects of a Chalkophore, Methanobactin, on Microbial Methylation of Mercury

Citation Formats

References (46)

Similar Records

Related Subjects