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.

  • Letter
  • Published:

Contaminant mobilization by metallic copper and metal sulphide colloids in flooded soil

Nature Geoscience volume 2, pages 267–271 (2009)Cite this article

Abstract

Colloids, such as submicrometre mineral particles or bacterial cells, can act as carriers enhancing the mobility of poorly soluble contaminants in subsurface environments1,2. In sulphate-reducing soils and sediments, metal sulphide precipitation has been proposed3,4,5,6 to generate contaminant-bearing sulphide colloids, which could transport contaminants traditionally thought to be immobilized by metal sulphide formation7. However, direct evidence for such a process is lacking. Here, we report the composition and morphology of pore-water colloids formed in contaminated floodplain soil when flooded with synthetic river water over a four-week period. We show that, on flooding, bacteria dispersed in the pore water mobilize copper by inducing biomineralization of metallic copper(0). We suggest that copper(0) crystals form by disproportionation of copper(I), which is released by copper-stressed bacteria to maintain copper homeostasis8,9. Sulphate reduction, which started on the fourth day of flooding, resulted in the mobilization of cadmium and lead, which were partitioned to copper-rich sulphide colloids showing two types of morphology: bacterium-associated ∼50–150-nm-diameter hollow particles formed through copper(0) transformation, and dispersed <50 nm nanoparticles, probably formed through homogeneous precipitation. The slow deposition of both types of sulphide colloid ensured elevated contaminant concentrations in the pore water for weeks. Our findings imply that colloid formation can enhance contaminant release from periodically sulphate-reducing soils and sediments, potentially polluting surface- and groundwaters.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Temporal dynamics of the pore-water composition during flooding.
Figure 2: Temporal evolution of Cu speciation.
Figure 3: Temporal evolution of colloid morphology and composition.
Figure 4: Inhibitors of Cu(0) biomineralization.

Similar content being viewed by others

References

  1. McCarthy, J. F. & Zachara, J. M. Subsurface transport of contaminants. Environ. Sci. Tech. 23, 496–502 (1989).

    Google Scholar 

  2. Kretzschmar, R., Borkovec, M., Grolimund, D. & Elimelech, M. Mobile subsurface colloids and their role in contaminant transport. Adv. Agron. 66, 121–193 (1999).

    Article  Google Scholar 

  3. Horzempa, L. M. & Helz, G. R. Controls on the stability of sulfide soils: Colloidal covellite as an example. Geochim. Cosmochim. Acta 43, 1645–1650 (1979).

    Article  Google Scholar 

  4. Gammons, C. H. & Frandsen, A. K. Fate and transport of metals in H2S-rich waters at a treatment wetland. Geochem. Trans. 2, 1–15 (2001).

    Article  Google Scholar 

  5. Moreau, J. W., Webb, R. I. & Banfield, J. F. Ultrastructure, aggregation-state, and crystal growth of biogenic nanocrystalline sphalerite and wurtzite. Am. Mineral. 89, 950–960 (2004).

    Article  Google Scholar 

  6. Lau, B. L. T. & Hsu-Kim, H. Precipitation and growth of zinc sulfide nanoparticles in the presence of thiol-containing natural organic ligands. Environ. Sci. Tech. 42, 7236–7241 (2008).

    Article  Google Scholar 

  7. Kirk, G. The Biogeochemistry of Submerged Soils (Wiley, 2004).

    Book  Google Scholar 

  8. Rensing, C. & Grass, G. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol. Rev. 27, 197–213 (2003).

    Article  Google Scholar 

  9. Outten, F. W., Huffman, D. L., Hale, J. A. & O’Halloran, T. V. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J. Biol. Chem. 276, 30670–30677 (2001).

    Article  Google Scholar 

  10. Hochella, M. F. Jr. et al. Direct observation of heavy metal–mineral association from the Clark Fork River Superfund Complex: Implications for metal transport and bioavailability. Geochim. Cosmochim. Acta 69, 1651–1663 (2005).

    Article  Google Scholar 

  11. Voegelin, A., Weber, F.-A. & Kretzschmar, R. Distribution and speciation of arsenic around roots in a contaminated riparian floodplain soil: Micro-XRF element mapping and EXAFS spectroscopy. Geochim. Cosmochim. Acta 71, 5804–5820 (2007).

    Article  Google Scholar 

  12. Luther, G. W. III & Rickard, D. T. Metal sulfide cluster complexes and their biogeochemical importance in the environment. J. Nanopart. Res. 7, 389–407 (2005).

    Article  Google Scholar 

  13. Rozan, T. F., Lassman, M. E., Ridge, D. P. & Luther, G. W. III. Evidence for iron, copper and zinc complexation as multinuclear sulphide clusters in oxic rivers. Nature 406, 879–882 (2000).

    Article  Google Scholar 

  14. Luther, G. W. III. et al. Aqueous copper sulfide clusters as intermediates during copper sulfide formation. Environ. Sci. Tech. 36, 394–402 (2002).

    Article  Google Scholar 

  15. Ferris, F. G., Fyfe, W. S. & Beveridge, T. J. Bacteria as nucleation sites for authigenic minerals in a metal-contaminated lake sediment. Chem. Geol. 63, 225–232 (1987).

    Article  Google Scholar 

  16. Bebie, J., Schoonen, M. A. A., Fuhrmann, M. & Strongin, D. R. Surface charge development on transition metal sulfides: An electrokinetic study. Geochim. Cosmochim. Acta 62, 633–642 (1998).

    Article  Google Scholar 

  17. Tufenkji, N. Modeling microbial transport in porous media: Traditional approaches and recent developments. Adv. Water Resour. 30, 1455–1469 (2007).

    Article  Google Scholar 

  18. Gustafsson, Ö. & Gschwend, P. M. Aquatic colloids: Concepts, definitions, and current challenges. Limnol. Oceanogr. 42, 519–528 (1997).

    Article  Google Scholar 

  19. Gschwend, P. M. & Reynolds, M. D. Monodisperse ferrous phosphate colloids in an anoxic groundwater plume. J. Contam. Hydrol. 1, 309–327 (1987).

    Article  Google Scholar 

  20. Jacobs, L., Emerson, S. & Skei, J. Partitioning and transport of metals across the O2/H2S interface in a permanently anoxic basin: Framvaren Fjord, Norway. Geochim. Cosmochim. Acta 49, 1433–1444 (1985).

    Article  Google Scholar 

  21. Lowry, G. V., Shaw, S., Kim, C. S., Rytuba, J. J. & Brown, G. E. Jr. Macroscopic and microscopic observations of particle-facilitated mercury transport from New Idria and Sulphur Bank mercury mine tailings. Environ. Sci. Tech. 38, 5101–5111 (2004).

    Article  Google Scholar 

  22. Kau, L.-S., Spira-Solomon, D. J., Penner-Hahn, J. E., Hodgson, K. O. & Solomon, E. I. X-ray absorption edge determination of the oxidation state and coordination number of copper: Application to the type 3 site in Rhus vernicifera laccase and its reaction with oxygen. J. Am. Chem. Soc. 109, 6433–6442 (1987).

    Article  Google Scholar 

  23. Peariso, K., Huffman, D. L., Penner-Hahn, J. E. & O’Halloran, T. V. The PcoC copper resistance protein coordinates Cu(I) via novel S-methionine interactions. J. Am. Chem. Soc. 125, 342–343 (2003).

    Article  Google Scholar 

  24. Davis, A. V. & O’Halloran, T. V. A place for thioether chemistry in cellular copper ion recognition and trafficking. Nature Chem. Biol. 4, 148–151 (2008).

    Article  Google Scholar 

  25. Manceau, A. et al. Formation of metallic copper nanoparticles at the soil–root interface. Environ. Sci. Tech. 42, 1766–1772 (2008).

    Article  Google Scholar 

  26. Reith, F., Lengke, M. F., Falconer, D., Craw, D. & Southam, G. The geomicrobiology of gold. ISME J. 1, 567–584 (2007).

    Article  Google Scholar 

  27. Pattrick, R. A. D. et al. The structure of amorphous copper sulfide precipitates: An X-ray absorption study. Geochim. Cosmochim. Acta 61, 2023–2036 (1997).

    Article  Google Scholar 

  28. Yin, Y. Formation of hollow nanocrystals through the nanoscale Kirkendall effect. Science 304, 711–714 (2004).

    Article  Google Scholar 

  29. Moreau, J. W. et al. Extracellular proteins limit the dispersal of biogenic nanoparticles. Science 316, 1600–1603 (2007).

    Article  Google Scholar 

  30. Karlsson, T., Persson, P. & Skyllberg, U. Complexation of copper(II) in organic soils and in dissolved organic matter—EXAFS evidence for chelate ring structures. Environ. Sci. Tech. 40, 2623–2628 (2006).

    Article  Google Scholar 

Download references

Acknowledgements

We thank K. Barmettler for support in the laboratory, S. Mangold for assistance at the XAS beamline at ANKA, and U. Skyllberg and J. F. W. Mosselmans for sharing reference XAS spectra. We thank ANKA Angströmquelle Karlsruhe GmbH, Germany, for allocation of synchrotron beamtime and acknowledge the support of the Electron Microscopy Centre (EMEZ) of ETH Zurich, Switzerland. Funding from the Swiss State Secretariat for Education and Research (contract 03.0353-1) as a contribution to the EU project AquaTerra is acknowledged.

Author information

Author notes

  1. Andreas Voegelin

    Present address: Present address: Eawag, Swiss Federal Institute of Aquatic Science and Technology, Ueberlandstrasse 133, 8600 Duebendorf, Switzerland,

Authors and Affiliations

  1. Institute of Biogeochemistry and Pollutant Dynamics, ETH Zurich, CHN F23.2, 8092 Zurich, Switzerland

    Frank-Andreas Weber, Andreas Voegelin & Ruben Kretzschmar

  2. Eawag, Swiss Federal Institute of Aquatic Science and Technology, Ueberlandstrasse 133, 8600 Duebendorf, Switzerland

    Ralf Kaegi

Authors
  1. Frank-Andreas Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andreas Voegelin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ralf Kaegi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ruben Kretzschmar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.-A.W. designed and performed all experiments and measurements, evaluated the results and wrote the manuscript as part of his PhD thesis. A.V. conducted EXAFS analyses and contributed to writing. R.Ka. conducted TEM analyses. A.V. and R.Kr. initiated and supervised the project. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Andreas Voegelin.

Supplementary information

Supplementary Table S1

Supplementary Information (PDF 794 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weber, FA., Voegelin, A., Kaegi, R. et al. Contaminant mobilization by metallic copper and metal sulphide colloids in flooded soil. Nature Geosci 2, 267–271 (2009). https://doi.org/10.1038/ngeo476

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo476

This article is cited by

Search

Advanced 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