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Potential role of the Fe(III)-reducing bacteria Geobacter and Geothrix in controlling arsenic solubility in Bengal delta sediments

Published online by Cambridge University Press:  05 July 2018

F. S. Islam ,
C. Boothman ,
A. G. Gault ,
D. A. Polya  and
J. R. Lloyd
F. S. Islam
Affiliation:
School of Earth, Atmospheric and Environmental Sciences & Williamson Research Centre for Molecular Environmental Science, University of Manchester, Oxford Road, Manchester M13 9PL, UK
C. Boothman
Affiliation:
School of Earth, Atmospheric and Environmental Sciences & Williamson Research Centre for Molecular Environmental Science, University of Manchester, Oxford Road, Manchester M13 9PL, UK
A. G. Gault
Affiliation:
School of Earth, Atmospheric and Environmental Sciences & Williamson Research Centre for Molecular Environmental Science, University of Manchester, Oxford Road, Manchester M13 9PL, UK
D. A. Polya
Affiliation:
School of Earth, Atmospheric and Environmental Sciences & Williamson Research Centre for Molecular Environmental Science, University of Manchester, Oxford Road, Manchester M13 9PL, UK
J. R. Lloyd*
Affiliation:
School of Earth, Atmospheric and Environmental Sciences & Williamson Research Centre for Molecular Environmental Science, University of Manchester, Oxford Road, Manchester M13 9PL, UK
*
*E-mail: jon.lloyd@manchester.ac.uk
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Abstract

Previous studies from our laboratory have suggested a role for indigenous metal-reducing bacteria in the reduction of sediment-bound As(V), and have also shown that a stable enrichment culture of Fe(III)-reducing bacteria was able to mobilize arsenic (as As(III)) from sediments collected from West Bengal (Islam et al., 2004). To identify the Fe(III)-reducing bacteria that may play a role in the reduction of As(V) and mobilization of As(III), we made a detailed molecular analysis of this enrichment culture. It was dominated by a close relative of Geothrix fermentans, but the type strain of this organism was unable to conserve energy for growth via the dissimilatory reduction of As(V), or reduce As(V) present in a defined medium containing fumarate as the electron acceptor. Furthermore, when the cells were grown using soluble Fe(III)-citrate as an electron acceptor in the presence of As(V), bacterial Fe(III) reduction resulted in the precipitation of the Fe(II)-bearing mineral vivianite in 2 weeks. This was accompanied by the efficient removal of As from solution. These results demonstrate that Geothrix fermentans, in common with other key Fe(III)-reducing bacteria such as Geobacter sulfurreducens, does not reduce As(V) enzymatically, but can capture arsenic in Fe(II) minerals formed during respiration using Fe(III) as an electron acceptor. Thus, the reduction of arsenic-bearing Fe(III) oxide minerals is not sufficient to mobilize arsenic, but may result in the formation of Fe(II) biominerals that could potentially act as sinks for arsenic in sediments. Additional mechanisms, including dissimilatory As(V) reduction by other specialist anaerobic bacteria, are implicated in the mobilization of arsenic from sediments.

Keywords

BengalarsenicFe(III) reductionAs(V) reductiondissimilatory metal reductionbiogeochemistry
Type
Research Article
Information
Mineralogical Magazine , Volume 69 , Issue 5 , October 2005 , pp. 865 - 875
Copyright
Copyright © The Mineralogical Society of Great Britain and Ireland 2005

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References

Acharyya, S.K., Chakraborty, P., Lahiri, S., Raymahashay, B.C., Guha, S. and Bhowmik, A. (1999) Arsenic poisoning in the Ganges delta. Nature, 401, 545.CrossRefGoogle ScholarPubMed
Akai, J., Izumi, K., Fukuhara, H., Masuda, H., Nakano, S., Yoshimura, T., Ohfuji, H., Md, A.H. and Akai, K. (2004) Mineralogical and geomicrobiological investigations on groundwater arsenic enrichment in Bangladesh. Applied Geochemistry, 19, 215–230.CrossRefGoogle Scholar
Battey, M.H. (1990) Mineralogy for students 2nd edition. Longman Scientific and Technical, Essex, UK.Google Scholar
Berg, M., Tran, H.C., Nguyen, T.C., Pham, H.V., Schertenleib, R. and Giger, W. (2001) Arsenic contamination of groundwater and drinking Water in Vietnam: a human health threat. Environmental Science and Technology, 35, 2621–2626.CrossRefGoogle ScholarPubMed
BGS and DPHE (2001) Arsenic contamination of groundwater in Bangladesh (Kinniburgh, D.G. and Smedley, P.L. (editors). British Geological Survey Technical Report WC/00/19, British Geological Survey, Keyworth, Nottingham, UK.Google Scholar
Bose, P. and Sharma, A. (2002) Role of iron in controlling speciation and mobilization of arsenic in subsurface environment. Water Research, 36, 4916–4926.CrossRefGoogle ScholarPubMed
Chowdhury, T.R., Basu, G.K., Mandal, B.K., Biswas, B.K., Samanta, G., Chowdhury, U.K., Chanda, C.R., Lodh, D., Roy, S.L., Saha, K.C., Roy, S., Kabir, S., Quamruzzaman, Q. and Chakraborti, D. (1999) Arsenic poisoning in the Ganges delta. Nature, 401, 545–546.CrossRefGoogle ScholarPubMed
Coates, J.D., Ellis, D.J., Gaw, C.V. and Lovley, D.R. (1999) Geothrix fermentans gen. nov., sp nov., a novel Fe(III)-reducing bacterium from a hydrocarbon-contaminated aquifer. International Journal of Systematic Bacteriology, 49, 1615–1622.Google ScholarPubMed
Das, D., Chatterjee, A., Mandal, B.K., Samanta, G., Chanda, B. and Chakraborti, D. (1995) Arsenic in groundwater in six districts of West Bengal, India, the biggest arsenic calamity in the world. Part 2. Arsenic concentration in drinking water, hair, nail, urine, skin-scale and liver tissue (biopsy) of the affected people. Analyst, 120, 917–924.CrossRefGoogle Scholar
Das, D., Samanta, G., Mandal, B.K., Chowdhury, T.R., Chanda, C.R., Chowdhury, P.P., Basu, G.K. and Chakraborti, D. (1996) Arsenic in groundwater in six districts of West Bengal, India. Environmental Geochemistry and Health, 18, 5—15.CrossRefGoogle ScholarPubMed
Gault, A.G., Jana, J., Chakraborty, S., Mukherjee, P., Sarkar, M., Nath, B., Polya, D.A. and Chatterjee, D. (2005) Preservation strategies for inorganic arsenic species in high iron, low Eh groundwater from West Bengal, India. Analytical and Bioanalytical Chemistry, 381, 347–35.CrossRefGoogle Scholar
Goodbred, S.L. and Kuehl, S.A. (2000) Enormous Ganges-Brahmaputra sediment discharge during strengthened early Holocene monsoon. Geology, 28, 1083–108.2.0.CO;2>CrossRefGoogle Scholar
Harvey, C.F., Swartz, C.H., Badruzzaman, A.B.M., Keon-Blute, N., Yu, W., Ashraf, A.M., Jay, J., Beckie, R., Niedan, V., Brabander, D., Oates, P.M., Ashfaque, K.N., Islam, S., Hemond, H.F. and Ahmed, M.F. (2002) Arsenic mobility and ground-water extraction in Bangladesh. Science, 298, 1602–1606.CrossRefGoogle ScholarPubMed
Holmes, D.E., Finneran, K.T. and Lovley, D.R. (2002) Enrichment of Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer sediments. Applied and Environmental Microbiology, 68, 2300—2306.CrossRefGoogle ScholarPubMed
Horneman, A., van Geen, A., Kent, D.V., Mathe, P.E., Zheng, Y., Dhar, R.K., O'Connell, S., Hoque, M.A., Aziz, Z. and Shamsudduha, M. (2004) Decoupling of As and Fe release to Bangladesh groundwater under reducing conditions. Part I: Evidence from sediment profiles. Geochimica et Cosmochimica Acta, 68, 3459–3473.CrossRefGoogle Scholar
Islam, F.S., Pederick, R.L., Gault, A.G., Adams, L.K., Polya, D.A., Charnock, J.M. and Lloyd, J.R. Reduction of Fe(III) by Geobacter sulfurreducens and the capture of arsenic by biogenic Fe(II) minerals. Applied and Environmental Microbiology (in press).Google Scholar
Islam, F.S., Gault, A.G., Boothman, C., Polya, D.A., Charnock, J.M., Chatterjee, D. and Lloyd, J.R. (2004) Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature, 430, 68–71.CrossRefGoogle ScholarPubMed
Jain, C.K. and Ali, I. (2000) Arsenic: occurrence, toxicity and speciation techniques. Water Research, 34, 4304–4312.CrossRefGoogle Scholar
Lawson, M. (2005) Mineralogical controls on arsenic mobility in Bengali and SE Asian groundwaters. Unpublished BSc (Hons) dissertation, School of Earth Atmospheric and Environmental Sciences, The University of Manchester, 48 pp.Google Scholar
Lloyd, J.R. (2003) Microbial reduction of metals and radionuclides. FEMS Microbiology Reviews, 27, 411–425.CrossRefGoogle ScholarPubMed
Lloyd, J.R., Leang, C., Hodges Myerson, A.L., Ciufo, S., Sandier, S.J., Methe, B. and Lovley, D.R. (2003) Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome i. Geobacter sulfurreducens. Biochemical Journal, 369, 153—161.CrossRefGoogle Scholar
Lovley, D.R. and Phillips, E.J.P. (1986) Availability of ferric iron for microbial reduction in bottom sediments of the freshwater tidal Potomac River. Applied and Environmental Microbiology, 52, 751–757.CrossRefGoogle ScholarPubMed
Macy, J.M., Nunan, K., Hagen, K.D., Dixon, D.R., Harbour, P.J., Cahill, M. and Sly, L.I. (1996) Chrysiogenes arsenatis, gen. sp. nov., a new arsenate-respiring bacterium isolated from gold mine wastewater. International Journal of Systematic Bacteriology, 46, 1153–1157.CrossRefGoogle Scholar
Manning, B.A., Fendorf, S.E. and Goldberg, S. (1998) Surface structures and stability of arsenic(III) on goethite: spectroscopic evidence for inner-sphere complexes. Environmental Science and Technology, 32, 2383–2388.CrossRefGoogle Scholar
McArthur, J.M., Ravenscroft, P., Safiulla, S. and Thirlwall, M.F. (2001) Arsenic in groundwater: testing pollution mechanisms for sedimentary aquifers in Bangladesh. Water Resources Research, 37, 109–117.CrossRefGoogle Scholar
McArthur, J.M., Banerjee, D.M., Hudson-Edwards, K.A., Mishra, R., Purohit, R., Ravenscroft, P., Cronin, A., Howarth, R.J., Chatterjee, A., Talukder, T., Lowry, D., Houghton, S. and Chadha, D.K. (2004) Natural organic matter in sedimentary basins and its relation to arsenic in anoxic ground water: the example of West Bengal and its worldwide implications. Applied Geochemistry, 19, 1255–1293.CrossRefGoogle Scholar
Methe, B.A., Nelson, K.E., Eisen, J.A., Paulsen, I.T., Nelson, W., Heidelberg, J.F., Wu, D., Wu, M., Ward, N., Beanan, M.J., Dodson, R.J., Madupu, R., Brinkac, L.M., Daugherty, S.C., DeBoy, R.T., Durkin, A.S., Gwinn, M., Kolonay, J.F., Sullivan, S.A., Haft, D.H., Selengut, J., Davidsen, T.M., Zafar, N., White, O., Tran, B., Romero, C., Forberger, H.A., Weidman, J., Khouri, H., Feldblyum, T.V., Utterback, T.R., Van Aken, S.E., Lovley, D.R. and Fraser, C.M. (2003) Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science, 302, 1967–1969.CrossRefGoogle ScholarPubMed
Mukhopadhyay, R., Rosen, B., Phung, L. and Silver, S. (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiology Review, 26, 311.CrossRefGoogle ScholarPubMed
Nevin, K.P. and Lovley, D.R. (2000) Potential for nonenzymatic reduction of Fe(in) during microbial oxidation of organic matter coupled to Fe(III) reduction. Environmental Science and Technology, 34, 2472–247.CrossRefGoogle Scholar
Nevin, K.P. and Lovley, D.R. (2002) Mechanisms for accessing insoluble Fe(III) oxide during dissimilatory Fe(III) reduction b. Geothrix fermentans. Applied and Environmental Microbiology, 68, 2294–2299.CrossRefGoogle Scholar
Nickson, R., McArthur, J., Burgess, W., Ahmed, K.M., Ravenscroft, P. and Rahman, M. (1998) Arsenic poisoning of Bangladesh groundwater. Nature 395, 338.CrossRefGoogle ScholarPubMed
Nickson, R.T., McArthur, J.M., Ravenscroft, P., Burgess, W.G. and Ahmed, K.M. (2000) Mechanism of arsenic release to groundwater, Bangladesh and West Bengal. Applied Geochemistry, 15, 403–413.CrossRefGoogle Scholar
Nickson, R.T., McArthur, J.M., Shrestha, B., Kyaw-Myint, T.O. and Lowry, D. (2005) Arsenic and other drinking water quality issues, Muzaffargarh District, Pakistan. Applied Geochemistry, 20, 55–68.CrossRefGoogle Scholar
Oremland, R.S. and Stolz, J.F. (2003) The ecology of arsenic. Science, 300, 939–944.CrossRefGoogle ScholarPubMed
Parkhurst, D.L. and Appelo, C.A.J. (1999) User's guide to PHREEQC (Version 2.) - A computer program for speciation, batch-reaction, one-dimensional transport and inverse geochemical calculations. US Geological Survey Water Resource Inv., 99-4259, 326 pp.Google Scholar
Pierce, M.L. and Moore, C.B. (1980) Adsorption of arsenite on amorphous iron hydroxide from dilute aqueous solution. Environmental Science and Technology, 14, 214–216.CrossRefGoogle Scholar
Pierce, M.L. and Moore, C.B. (1982) Adsorption of arsenite and arsenate on amorphous iron hydroxide. Water Research, 16, 1247–1253.CrossRefGoogle Scholar
Polya, D.A. (1998) TRPEAK. Unpublished manuscript, Department of Earth Sciences, University of Manchester, UK.Google Scholar
Polya, D.A. (1999) DBSCORR. Unpublished manuscript, Department of Earth Sciences, University of Manchester, UK.Google Scholar
Polya, D.A., Gault, A.G., Bourne, N.J., Lythgoe, P.R. and Cooke, D.A. (2003) Coupled HPLC-ICP-MS analysis indicates highly hazardous concentrations of dissolved arsenic species are present in Cambodian wellwaters. Pp. 127–140 in: Plasma Source Mass Spectrometry: Applications and Emerging Technologies (Holland, J.G. and Tanner, S.D., editors). The Royal Society of Chemistry, Cambridge, UK.CrossRefGoogle Scholar
Polya, D.A., Gault, A.G., Diebe, N., Feldman, P., Rosenboom, J.-W., Gilligan, E., Fredericks, D., Milton, A.H., Samson, M., Rowland, H.A.L., Lythgoe, P.R., Jones, J.C., Middleton, C. and Cooke, D.A. (2005) Arsenic hazard in shallow Cambodian groundwaters. Mineralogical Magazine, 69, 807–823.CrossRefGoogle Scholar
Rowland, H.A.L., Gault, A.G., Charnock, J.M. and Polya, D.A. (2005) Preservation and XANES determination of the oxidation state of solid phase arsenic species in shallow sedimentary aquifers in Bengal and Cambodia. Mineralogical Magazine, 69, 825–839.CrossRefGoogle Scholar
Smedley, P.L. and Kinniburgh, D.G. (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Applied Geochemistry, 17, 517—568.CrossRefGoogle Scholar
Smedley, P.L., Kinniburgh, D.G., MacDonald, D.M.J., Nicolli, H.B., Barros, A.J., Tullio, J.O., Pearce, J.M. and Alonso, M.S. (2005) Arsenic association in sediments from the loess aquifer of La Pampa, Argentina. Applied Geochemistry, 20, 989–1017.CrossRefGoogle Scholar
Smith, A.H., Lingas, E.O. and Rahman, M. (2000) Contamination of drinking-water by arsenic in Bangladesh: a public health emergency. Bulletin WHO, 78, 1093–1103.Google ScholarPubMed
Snoeyenbos-West, O., Nevin, K.P., Anderson, R.T. and Lovley, D.R. (2000) Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microbial Ecology, 39, 153–167.CrossRefGoogle ScholarPubMed
van Geen, A., Rose, J., Thoral, S., Gamier, J.M., Zheng, Y. and Bottero, J.Y. (2004) Decoupling of As and Fe release to Bangladesh groundwater under reducing conditions. Part II: Evidence from sediment incubations. Geochimica et Cosmochimica Acta, 68, 3475–3486.CrossRefGoogle Scholar
Zobrist, J., Dowdle, P.R., Davis, J.A. and Oremland, R.S. (2000) Mobilization of arsenite by dissimilatory reduction of adsorbed arsenate. Environmental Science and Technology, 34, 4747–4753.CrossRefGoogle Scholar