Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

High methylation rates of mercury bound to cysteine by Geobacter sulfurreducens

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

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Effect of cysteine on mercury methylation.
Figure 2: In vivo and in vitro mercury methylation rates in the presence of different thiols.
Figure 3: Hg(II) uptake and methylation by G. sulfurreducens in the presence of various thiols.

Similar content being viewed by others

References

  1. Choi, S.-C., Chase, T. Jr & Bartha, R. Enzymatic catalysis of mercury methylation by Desulfovibrio desulfuricans LS. Appl. Environ. Microbiol. 60, 1342–1346 (1994).

    Google Scholar 

  2. 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).

    Article  Google Scholar 

  3. 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).

    Article  Google Scholar 

  4. Clarkson, T. W. Human toxicology of mercury. J. Trace. Elem. Exp. Med. 11, 303–317 (1998).

    Article  Google Scholar 

  5. Compeau, G. C. & Bartha, R. Sulfate-reducing bacteria: Principal methylators of mercury in anoxic estuarine sediment. Appl. Environ. Microbiol. 50, 498–502 (1985).

    Google Scholar 

  6. Gilmour, C. C., Henry, E. A. & Mitchell, R. Sulfate stimulation of mercury methylation in freshwater sediments. Environ. Sci. Tech. 26, 2281–2287 (1992).

    Article  Google Scholar 

  7. 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).

    Article  Google Scholar 

  8. Kerin, E. J. et al. Mercury methylation by dissimilatory iron-reducing bacteria. Appl. Environ. Microbiol. 72, 7919–7921 (2006).

    Article  Google Scholar 

  9. 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).

    Google Scholar 

  10. 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).

    Article  Google Scholar 

  11. 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).

    Article  Google Scholar 

  12. 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).

    Article  Google Scholar 

  13. 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).

    Article  Google Scholar 

  14. Lenz, G. R. & Martell, A. E. Metal chelates of some sulfur-containing amino acids. Biochemistry 3, 745–750 (1964).

    Article  Google Scholar 

  15. Strand, R., Lund, W. & Aaseth, J. Complex formation of zinc, cadmium, and mercury with penicillamine. J. Inorg. Biochem. 19, 301–309 (1983).

    Article  Google Scholar 

  16. Kõszegi-Szalai, H. & Paál, T. L. Equilibrium studies of mercury(II) complexes with penicillamine. Talanta 48, 393–402 (1999).

    Article  Google Scholar 

  17. 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).

    Article  Google Scholar 

  18. 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).

    Article  Google Scholar 

  19. 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).

    Article  Google Scholar 

  20. Gilmour, C. C. et al. Methylmercury concentrations and production rates across a trophic gradient in the northern Everglades. Biogeochemistry 40, 327–345 (1998).

    Article  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Jeffra K. Schaefer.

Supplementary information

Supplementary Information, Fig SI-1

Supplementary Information (PDF 144 kb)

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo412

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing