Substantial contribution of biomethylation to aquifer arsenic cycling

Journal name:
Nature Geoscience
Volume:
8,
Pages:
290–293
Year published:
DOI:
doi:10.1038/ngeo2383
Received
Accepted
Published online

Microbes play a prominent role in transforming arsenic to and from immobile forms in aquifers1. Much of this cycling involves inorganic forms of arsenic2, but microbes can also generate organic forms through methylation3, although this process is often considered insignificant in aquifers4, 5, 6, 7. Here we identify the presence of dimethylarsinate and other methylated arsenic species in an aquifer hosted in volcaniclastic sedimentary rocks. We find that dimethylarsinate is widespread in the aquifer and its concentration correlates strongly with arsenite concentration. We use laboratory incubation experiments and an aquifer injection test to show that aquifer microbes can produce dimethylarsinate at rates of about 0.1% of total dissolved arsenic per day, comparable to rates of dimethylarsinate production in surface environments. Based on these results, we estimate that globally, biomethylation in aquifers has the potential to transform 100 tons of inorganic arsenic to methylated arsenic species per year, compared with the 420–1,250 tons of inorganic arsenic that undergoes biomethylation in soils8. We therefore conclude that biomethylation could contribute significantly to aquifer arsenic cycling. Because biomethylation yields arsine and methylarsines, which are more volatile and prone to diffusion than other arsenic species, we further suggest that biomethylation may serve as a link between surface and subsurface arsenic cycling.

At a glance

Figures

  1. Correlation between DMA(V) and arsenite in the bedrock aquifer.
    Figure 1: Correlation between DMA(V) and arsenite in the bedrock aquifer.

    The symbols show the results of the chemical analysis; the line represents the best fit.

  2. Variations with time in arsenic concentrations during aquifer injection test.
    Figure 2: Variations with time in arsenic concentrations during aquifer injection test.

    The symbols show the results of the chemical analysis; the dashed lines show the hypothetical concentrations under the assumption that only groundwater mixing occurred.

  3. Variations in methylarsenical concentration with total arsenic concentration in aquifers contaminated naturally with arsenic.
    Figure 3: Variations in methylarsenical concentration with total arsenic concentration in aquifers contaminated naturally with arsenic.

    Methylarsenicals include monomethylarsonate and dimethylarsinate; in the shaded area, methylarsenicals account for 0.1 to 10% of total arsenic. Open symbols are individual data points from aquifers of the Murshidabad district of West Bengal ( )13; Datong ( )14 and Inner Mongolia ( )15 of China; Taiwan ( )16; Cyprus ( )17; Argentina ( )18; and Florida ( ) 20, New Jersey ( ) 21 and Oregon ( , this study) of the USA. Filled symbols represent average concentrations in the aquifers of Mexico ( )19 and the Nadia district of West Bengal ( )12; error bars show standard deviation.

References

  1. Mukhopadhyay, R., Rosen, B. P., Phung, L. T. & Silver, S. Microbial arsenic: From geocycles to genes and enzymes. FEMS Microbiol. Rev. 26, 311325 (2002).
  2. Zhu, Y-G., Yoshinaga, M., Zhao, F-J. & Rosen, B. P. Earth abides arsenic biotransformations. Annu. Rev. Earth Planet Sci. 42, 443467 (2014).
  3. Bentley, R. & Chasteen, T. G. Microbial methylation of metalloids: Arsenic, antimony, and bismuth. Microbiol. Mol. Biol. Rev. 66, 250271 (2002).
  4. Lloyd, J. R. in Biological Chemistry of Arsenic, Antimony and Bismuth (ed. Sun, H.) Ch. 6, 135143 (Wiley, 2010).
  5. Oremland, R. S. & Stolz, J. F. The ecology of arsenic. Science 300, 939944 (2003).
  6. Rhine, E. D., Garcia-Dominguez, E., Phelps, C. D. & Young, L. Y. Environmental microbes can speciate and cycle arsenic. Environ. Sci. Technol. 39, 95699573 (2005).
  7. Lièvremont, D., Bertin, P. N. & Lett, M-C. Arsenic in contaminated waters: Biogeochemical cycle, microbial metabolism and biotreatment processes. Biochimie 91, 12291237 (2009).
  8. Mestrot, A. et al. Field fluxes and speciation of arsines emanating from soils. Environ. Sci. Technol. 45, 17981804 (2011).
  9. Islam, F. S. et al. Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature 430, 6871 (2004).
  10. Qin, J. et al. Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc. Natl Acad. Sci. USA 103, 20752080 (2006).
  11. Wood, J. M. Biological cycles for toxic elements in the environment. Science 183, 10491052 (1974).
  12. Gault, A. G. et al. in Plasma Source Mass Spectrometry: Applications and Emerging Technologies (eds Holland, G. & Tanner, S. D.) 112126 (Royal Society of Chemistry, 2003).
  13. Shraim, A., Sekaran, N. C., Anuradha, C. D. & Hirano, S. Speciation of arsenic in tube-well water samples collected from West Bengal, India, by high-performance liquid chromatography–inductively coupled plasma mass spectrometry. Appl. Organomet. Chem. 16, 202209 (2002).
  14. Xie, X. et al. Geochemistry of redox-sensitive elements and sulfur isotopes in the high arsenic groundwater system of Datong Basin, China. Sci. Total Environ. 407, 38233835 (2009).
  15. Lin, N-F., Tang, J. & Bian, J-M. Characteristics of environmental geochemistry in the arseniasis area of the Inner Mongolia of China. Environ. Geochem. Health 24, 249259 (2002).
  16. Lin, T-H., Huang, Y-L. & Ming-Yuh, W. Arsenic species in drinking water, hair, fingernails, and urine of patients with blackfoot disease. J. Toxicol. Environ. Health A 53, 8593 (1998).
  17. Christodoulidou, M. et al. Arsenic concentrations in groundwaters of Cyprus. J. Hydrol. 468–469, 94100 (2012).
  18. Watts, M. J., OReilly, J., Marcilla, A. L., Shaw, R. A. & Ward, N. I. Field based speciation of arsenic in UK and Argentinean water samples. Environ. Geochem. Health 32, 479490 (2010).
  19. Del Razo, L. M., Arellano, M. A. & Cebrián, M. E. The oxidation states of arsenic in well-water from a chronic arsenicism area of Northern Mexico. Environ. Pollut. 64, 143153 (1990).
  20. Braman, R. S. & Foreback, C. C. Methylated forms of arsenic in the environment. Science 182, 12471249 (1973).
  21. Serfes, M. E., Spayd, S. E. & Herman, G. C. in Advances in Arsenic Research Vol. 915 (eds Oday, P. A., Vlassopoulos, D., Meng, X. & Benning, L. G.) Ch. 13, 175190 (ACS Symposium Series, American Chemical Society, 2005).
  22. Gannett, M. W. & Caldwell, R. R. Geologic Framework of the Willamette Lowland Aquifer System, Oregon and Washington (US Geological Survey, 1998).
  23. Istok, J. D., Humphrey, M. D., Schroth, M. H., Hyman, M. R. & OReilly, K. T. Single-well, ‘push-pull test for in situ determination of microbial activities. Ground Water 35, 619631 (1997).
  24. Lafferty, B. J. & Loeppert, R. H. Methyl arsenic adsorption and desorption behavior on iron oxides. Environ. Sci. Technol. 39, 21202127 (2005).
  25. Aurilio, A. C., Mason, R. P. & Hemond, H. F. Speciation and fate of arsenic in three lakes of the Aberjona Watershed. Environ. Sci. Technol. 28, 577585 (1994).
  26. Sohrin, Y., Matsui, M., Kawashima, M., Hojo, M. & Hasegawa, H. Arsenic biogeochemistry affected by eutrophication in Lake Biwa, Japan. Environ. Sci. Technol. 31, 27122720 (1997).
  27. Smedley, P. L. & Kinniburgh, D. G. A review of the source, behaviour and distribution of arsenic in natural waters. Appl. Geochem. 17, 517568 (2002).
  28. Koide, H. et al. Subterranean containment and long-term storage of carbon dioxide in unused aquifers and in depleted natural gas reservoirs. Energy Convers. Manage. 33, 619626 (1992).
  29. Chilvers, D. & Peterson, P. in Lead, Mercury, Cadmium and Arsenic in the Environment (eds Hutchinson, T. C. & Meema, K. M.) Ch. 17, 279301 (Wiley, 1987).
  30. Akter, K. F., Owens, G., Davey, D. E. & Naidu, R. Arsenic speciation and toxicity in biological systems. Rev. Environ. Contam. Toxicol. 184, 97149 (2005).

Download references

Author information

Affiliations

  1. Department of Geological Sciences, University of Oregon, Eugene, Oregon 97403, USA

    • Scott C. Maguffin,
    • Ashley R. Daigle &
    • Qusheng Jin
  2. Department of Geology, Kansas State University, Manhattan, Kansas 66506, USA

    • Matthew F. Kirk
  3. US Geological Survey, Portland, Oregon 97201, USA

    • Stephen R. Hinkle

Contributions

Q.J. and S.R.H. designed the project. Q.J. compiled previous studies of groundwater methylarsenicals. Q.J. and M.F.K. conducted the field sampling and analysis. S.C.M. carried out the laboratory experiments. Q.J. and A.R.D. carried out the aquifer test. Q.J. wrote the manuscript, with significant input from S.R.H. and M.F.K.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

Author details

Supplementary information

PDF files

  1. Supplementary Information (5,930 KB)

    Supplementary Information

Additional data