Abstract
Methylmercury bioaccumulates in aquatic food chains and is able to cross the blood–brain barrier, making this organometallic compound a much more worrisome pollutant than inorganic mercury. We know that methylation of inorganic mercury is carried out by microbes in the anoxic layers of sediments and water columns, but the factors that control the extent of this methylation are poorly known. Mercury methylation is generally thought to be catalysed accidentally by some methylating enzyme1,2, and it has been suggested that cellular mercury uptake results from passive diffusion of neutral mercury complexes3. Here, we show that mercury methylation by the bacterium Geobacter sulfurreducens is greatly enhanced in the presence of low concentrations of the amino acid cysteine. The formation of a mercury–cysteine complex promotes both the uptake of inorganic mercury by the bacteria and the enzymatic formation of methylmercury, which is subsequently released to the external medium. Our results suggest that mercury uptake and methylation by microbes are controlled more tightly by biological mechanisms than previously thought, and that the formation of specific mercury complexes in anoxic waters modulates the efficiency of the microbial methylation of mercury.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Choi, S.-C., Chase, T. Jr & Bartha, R. Enzymatic catalysis of mercury methylation by Desulfovibrio desulfuricans LS. Appl. Environ. Microbiol. 60, 1342–1346 (1994).
Ekstrom, E. B., Morel, F. M. M. & Benoit, J. M. Mercury methylation independent of the acetyl-coenzyme A pathway in sulfate-reducing bacteria. Appl. Environ. Microbiol. 69, 5414–5422 (2003).
Benoit, J. M., Gilmour, C. C. & Mason, R. P. Aspects of bioavailability of mercury for methylation in pure cultures of Desulfobulbus propionicus (1pr3). Appl. Environ. Microbiol. 67, 51–58 (2001).
Clarkson, T. W. Human toxicology of mercury. J. Trace. Elem. Exp. Med. 11, 303–317 (1998).
Compeau, G. C. & Bartha, R. Sulfate-reducing bacteria: Principal methylators of mercury in anoxic estuarine sediment. Appl. Environ. Microbiol. 50, 498–502 (1985).
Gilmour, C. C., Henry, E. A. & Mitchell, R. Sulfate stimulation of mercury methylation in freshwater sediments. Environ. Sci. Tech. 26, 2281–2287 (1992).
Fleming, E. J., Mack, E. E., Green, P. G. & Nelson, D. C. Mercury methylation from unexpected sources: Molybdate-inhibited freshwater sediments and an iron-reducing bacterium. Appl. Environ. Microbiol. 72, 457–464 (2006).
Kerin, E. J. et al. Mercury methylation by dissimilatory iron-reducing bacteria. Appl. Environ. Microbiol. 72, 7919–7921 (2006).
Benoit, J., Gilmour, C., Heyes, A., Mason, R. P. & Miller, C. in Biogeochemistry of Environmentally Important Trace Elements (eds Chai, Y. & Braids, O. C.) 262–297 (American Chemical Society, 2003).
Ullrich, S. M., Tanton, T. W. & Abdrashitova, S. A. Mercury in the aquatic environment: A review of factors affecting methylation. Crit. Rev. Environ. Sci. Tech. 31, 241–293 (2001).
Benoit, J. M., Gilmour, C. C., Mason, R. P. & Heyes, A. Sulfide controls on mercury speciation and bioavailability to methylating bacteria in sediment pore waters. Environ. Sci. Tech. 33, 951–957 (1999).
Skyllberg, U. Competition among thiols, inorganic sulfides and polysulfides for Hg and MeHg in wetland soils and sediments under suboxic conditions—illumination of controversies and implications for MeHg net production. J. Geophys. Res. 113, G00C03 (2008).
Casas, J. S. & Jones, M. M. Mercury(II) complexes with sulfhydryl containing chelating agents: Stability constant inconsistencies and their resolution. J. Inorg. Nucl. Chem. 42, 99–102 (1980).
Lenz, G. R. & Martell, A. E. Metal chelates of some sulfur-containing amino acids. Biochemistry 3, 745–750 (1964).
Strand, R., Lund, W. & Aaseth, J. Complex formation of zinc, cadmium, and mercury with penicillamine. J. Inorg. Biochem. 19, 301–309 (1983).
Kõszegi-Szalai, H. & Paál, T. L. Equilibrium studies of mercury(II) complexes with penicillamine. Talanta 48, 393–402 (1999).
Golding, G. R. et al. Evidence for facilitated uptake of Hg(II) by Vibrio anguillarum and Escherichia coli under anaerobic and aerobic conditions. Limnol. Oceanogr. 47, 967–975 (2002).
Bridges, C. C., Bauch, C., Verrey, F. & Zalups, R. K. Mercuric conjugates of cysteine are transported by the amino acid transporter system b0,+: Implications of molecular mimicry. J. Am. Soc. Nephrol. 15, 663–673 (2004).
Zhang, J., Wang, F., House, J. D. & Page, B. Thiols in wetland interstitial waters and their role in mercury and methylmercury speciation. Limnol. Oceanogr. 49, 2276–2286 (2004).
Gilmour, C. C. et al. Methylmercury concentrations and production rates across a trophic gradient in the northern Everglades. Biogeochemistry 40, 327–345 (1998).
Acknowledgements
We wish to thank C. Cobb-Adams for technical assistance. The research was supported by grants from the Electric Power Research Institute (EPRI) and the Center for Environmental and BioInorganic Chemistry (CEBIC) funded by NSF.
Author information
Authors and Affiliations
Corresponding author
Supplementary information
Supplementary Information, Fig SI-1
Supplementary Information (PDF 144 kb)
Rights and permissions
About this article
Cite this article
Schaefer, J., Morel, F. High methylation rates of mercury bound to cysteine by Geobacter sulfurreducens. Nature Geosci 2, 123–126 (2009). https://doi.org/10.1038/ngeo412
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ngeo412
This article is cited by
-
Metabolically diverse microorganisms mediate methylmercury formation under nitrate-reducing conditions in a dynamic hydroelectric reservoir
The ISME Journal (2023)
-
Impacts of spectral characteristics of dissolved organic matter on methylmercury contents in peatlands, Northeast China
Environmental Geochemistry and Health (2023)
-
Distribution and Release of Mercury Regulated by the Decomposition of a Pioneer Habitat-Adapted Plant in the Water-Level-Fluctuating Zone of the Three Gorges Reservoir
Bulletin of Environmental Contamination and Toxicology (2023)
-
Elevated methylmercury production in mercury-contaminated soil and its bioaccumulation in rice: key roles of algal decomposition
Frontiers of Environmental Science & Engineering (2023)
-
Effect of exogenous and endogenous sulfide on the production and the export of methylmercury by sulfate-reducing bacteria
Environmental Science and Pollution Research (2023)