Isolation and Characterization of NP4, Arsenate-Reducing Sulfurospirillum, from Maine Groundwater
Publication: Journal of Environmental Engineering
Volume 133, Issue 1
Abstract
Parts of New England have naturally high arsenic concentrations in groundwater. High arsenic correlates broadly with bedrock type, but levels are patchy, so other conditions must affect arsenic mobilization. Microorganisms capable of arsenate respiration, if present, could affect arsenic speciation and mobility in groundwater. An arsenate-reducing bacterium, designated NP4, was isolated from groundwater obtained from a well in Northport, Me., with extremely high arsenic. Sequencing of the 16S rDNA showed that NP4 groups with the Sulfurospirillum genus. It can grow using arsenate, nitrate, iron(III), selenate, manganese(IV), sulfite, sulfur or thiosulfate as terminal electron acceptors and lactate, formate and pyruvate as electron donors. It can also grow on fumarate or lactate alone. This Sulfurospirillum isolate is distinct from other members of the genus in its carbon and electron acceptor usage. The activity of this type of microorganism could negatively affect groundwater quality by converting to the more toxic and difficult to remove form.
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Acknowledgments
This material is based upon work supported by the National Science Foundation under Grant No. NSF0134054 and the USGS WRRI program. The writers thank Dr. Katherine Boettcher for initially amplifying the NP4 DNA, Dr. Brian Perkins for assistance with the HPLC, and Cheng Chen for assistance in the laboratory.
References
Altschul, S. F., et al. (1997). “Gapped BLAST and PSI-BLAST: A new generation of protein database search programs.” Nucleic Acids Res., 25(17), 3389–3402.
American Public Health Association (APHA), American Water Works Association (AWWA), and Water Environment Foundation (WEF) (1998). Standard methods for the examination of water and wastewater, 20th ed., Washington, D.C.
Ayotte, J. D., et al. (2006). “Modeling the probability of arsenic in groundwater in New England as a tool for exposure assessment.” Environ. Sci. Technol., in press.
Ayotte, J. D., Montgomery, D. L., Flanagan, S. M., and Robinson, K. W. (2003). “Arsenic in groundwater in eastern New England: Occurrence, controls and human health implications.” Environ. Sci. Technol., 37(10), 2075–2083.
Ayotte, J. D., Nielsen, M. G., Robinson, G. R., Jr., and Moore, R. B. (1999). Relation of arsenic, iron and manganese in ground water to aquifer type, bedrock lithogeochemistry, and land use in the New England coastal basins, Water-Resources Investigation Report 99-4162, National Water Quality Assessment Program, U.S. Dept. Interior, USGS, Washington, D.C.
Beveridge, T. J., Popkin, T. J., and Cole, R. M. (1994). “Electron microscopy.” Methods for general and molecular bacteriology, P. Gerhardt, R. G. E. Murray, W. A. Wood, and N. R. Krieg, eds., American Society for Microbiology, Washington, D.C., 42–71.
Bose, P., and Sharma, A. (2002). “Role of iron in controlling speciation and mobilization of arsenic in subsurface environment.” Water Res., 36(19), 4916–4926.
Breznak, J. A., and Costilow, R. N. (1994). “Physicochemical factors in growth.” Methods for general and molecular bacteriology, P. Gerhardt, R. G. E. Murray, W. A. Wood, and N. R. Krieg, eds., American Society for Microbiology, Washington, D.C., 148–149.
Charlet, L., Ansari, A. A., Lespagnol, M., and Musso, M. (2001). “Risk of arsenic transfer to a semi-confined aquifer and the effect of water level fluctuation in North Montagne, France at a former industrial site.” Sci. Total Environ., 27(1–3), 133–147.
Culbertson, C. W., Strohmaier, F. E., and Oremland, R. S. (1988). “Acetylene as a substrate in the development of primordial bacterial communities.” Origins Life Evol. Biosphere, 18(4), 397–407.
Farquhar, M. L., Charnock, J. M., Livens, F. R., and Vaughan, D. J. (2002). “Mechanisms of arsenic uptake from aqueous solution by interaction with goethite, lepidocrite, mackinawite, and pyrite: An X-ray absorption spectroscopy study.” Environ. Sci. Technol., 36(8), 1757–1762.
Giovannoni, S. (1991). “Polymerase chain reaction.” Nucleic acid techniques in bacterial systematics, E. Stackebrandt and M. Goodfellow, eds., Wiley, New York, 177–204.
Hering, J. G., Chen, P.-Y., Wilkie, J. A., and Elimelech, M. (1997). “Arsenic removal from drinking water during coagulation.” J. Environ. Eng., 123(8), 800–807.
Islam, F. S., et al. (2004). “Role of metal reducing bacteria in arsenic release from Bengal delta sediments.” Nature, 430(6995), 68–71.
Karner, M. B., DeLong, E. F., and Karl, D. M. (2001). “Archaeal dominance in the mesopelagic zone of the Pacific Ocean.” Nature, 409(6819), 507–510.
Kartinen, E. O., Jr., and Martin, C. J. (1995). “An overview of arsenic removal processes.” Desalination, 103(1), 79–88.
Lane, D. J. (1991). “16S/23S rRNA sequencing.” Nucleic acid techniques in bacterial systematics, E. Stackebrandt and M. Goodfellow, eds., Wiley, New York, 115–176.
Langner, H. W., Jackson, C. R., McDermott, T. R., and Inskeep, W. P. (2001). “Rapid oxidation of arsenite in a hot spring ecosystem, Yellowstone National Park.” Environ. Sci. Technol., 35(16), 3302–3309.
Laverman, A. M., Switzer Blum, J., Schaefer, J. K., Phillips, E. J. P., Lovley, D. R., and Oremland, R. S. (1995). “Growth of SES-3 with arsenate and other diverse electron acceptors.” Appl. Environ. Microbiol., 61(10), 3556–3561.
Lipfert, G., Reeve, A. S., Sidle, W. C., and Marvinney, R. (2006). “Geochemical patterns of arsenic-enriched ground-water in fractured, crystalline bedrock, Northport, Maine, USA.” Appl. Geochem., 21(3), 528–545.
Loiselle, M. C., Marvinney, R. G., and Smith, A. E. (2002). “Arsenic in groundwater wells in Maine.” Proc., 2002 Arsenic in New England Conf., Manchester, N.H.⟨http://www.dartmouth.edu/~cehs/ArsenicConference/loiselle.html⟩.
Lovely, D. R., Coates, J. D., Blunt-Harris, E. L., Philips, E. J. P., and Woodward, J. C. (1996). “Humic substances as electron acceptors for microbial respiration.” Nature (London), 382(6590), 445–448.
Luijten, M. L. G. C., et al. (2003). “Description of Sulfurospirillum halorespirans sp. nov., an anaerobic, tetrachloroethene-respiring bacterium, and transfer of Dehalospirillum multivorans to the genus Sulfurospirillum as Sulfurospirillum multivorans, comb. nov.” Int. J. Syst. Evol. Microbiol., 53(3), 787–793.
Luijten, M. L. G. C., et al. (2004). “Anaerobic reduction and oxidation of quinine moieties and the reduction of oxidized metals by halorespiring and related organisms.” FEMS Microbiol. Ecol., 49(1), 145–150.
Matschullat, J. (2000). “Arsenic in the geosphere–a review.” Sci. Total Environ., 249(1–3), 297–312.
Meng, X., Korfiatis, G. P., Bang, S., and Bang, K. W. (2002). “Combined effect of anions on arsenic removal by iron hydroxides.” Toxicol. Lett., 133(1), 103–111.
Mukhopadhyay, R., Rosen, B. P., Phung, L. T., and Silver, S. (2002). “Microbial arsenic: From geocycles to genes and enzymes.” FEMS Microbiol. Rev., 26(3), 311–325.
Murray, R. G. E., and Robinow, C. F. (1994). “Light microscopy.” Methods for general and molecular bacteriology, P. Gerhardt, R. G. E. Murray, W. A. Wood, and N. R. Krieg, eds., American Society for Microbiology, Washington, D.C., 7–20.
Newman, D. K., Ahmann, D., and Morel, F. M. M. (1998). “A brief review of microbial arsenate respiration.” Geomicrobiol. J., 15(4), 255–268.
Ning, R. Y. (2002). “Arsenic removal by reverse osmosis.” Desalination, 143(3), 237–241.
Oremland, R. S., and Stolz, J. F. (2005). “Arsenic, microbes and contaminated aquifers.” Trends Microbiol., 13(2), 45–49.
Redman, A., Macalady, D. L., and Ahmann, D. (2002). “Natural organic matter affects arsenic speciation and sorption onto hematite.” Environ. Sci. Technol., 36(13), 2889–2896.
Rittman, B. E., and McCarty, P. L. (2001). “Stoichiometry and bacterial energetics.” Environmental biotechnology: Principles and applications, Chap. 2, McGraw-Hill, Boston, 126–164.
Rosen, B. P. (2002). “Biochemistry of arsenic detoxification.” FEBS Lett., 529(1), 86–92.
Scholz-Muramatsu, H., Neumann, A., Meßmer, M., Moore, E., and Diekert, G. (1995). “Isolation and characterization of Dehalospirillum multivorans gen. nov., sp. nov., a tetrachloroethene-utilizing, strictly anaerobic bacterium.” Arch. Microbiol., 163(1), 48–56.
Smedley, P. L., and Kinniburgh, D. G. (2002). “A review of the source, behaviour and distribution of arsenic in natural waters.” Appl. Geochem., 7(5), 517–568.
Smith, A. H., Lingas, E. O., and Rahman, M. (2000). “Contamination of drinking water by arsenic in Bangladesh: A public health emergency.” Bull. World Health Organ, 78(9), 1093–1103.
Smith, E., Naidu, R., and Alston, A. M. (1998). “Arsenic in the soil environment.” Adv. Agronomy, 64, 149–195.
Stolz, J. F., Ellis, D. J., Switzer Blum, J., Ahmann, D., Lovley, D. R., and Oremland, R. S. (1999). “Sulfurospirillum barnseii sp. nov. and Sulfurospirillum arsenophilum sp. nov., new members of the Sulfurospirillum clade of the Proteobacteria.” Int. J. Syst. Bacteriol., 49(3), 1177–1180.
Stolz, J. F., and Oremland, R. S. (1999). “Bacterial respiration of arsenic and selenium.” FEMS Microbiol. Rev., 23(5), 615–627.
Straub, K. L., and Schink, B. (2004). “Ferrihydrite-dependent growth of Sulfurospirillum deleyianum through electron transfer vie sulfur cycling.” Appl. Environ. Microbiol., 70(10), 5744–5749.
Su, C., and Puls, R. W. (2001). “Arsenate and arsenite removal by zerovalent iron: kinetics, redox transformation and implications for in situ groundwater remediation.” Environ. Sci. Technol., 35(7), 1487–1492.
United States Environmental Protection Agency (USEPA). (1998). “Research plan for arsenic in drinking water.” EPA/600/R-98/042, Office of Research and Development, National Center for Environmental Assessment, Washington, D.C. http://www.epa.gov/ORD/WebPubs/final/arsenic.pdf .
United States Environmental Protection Agency (USEPA). (2000). “Technologies and costs for removal of arsenic from drinking water.” EPA 815-R-00-028 http://www.epa.gov/safewater/ars/treatments_and_costs.pdf .
Weldon, J., and MacRae, J. D. (2006). “Correlations between arsenic in Maine groundwater and microbial populations as determined by fluorescence in situ hybridization.” Chemosphere, 63(3), 440–448.
Wilkie, J. A., and Hering, J. G. (1996). “Adsorption of arsenic onto ferric oxide: effects of adsorbate/adsorbent ratios and co-occurring solutes.” Colloids Surf., A, 107, 97–110.
Wilkie, J. A., and Hering, J. G. (1998). “Rapid oxidation of geothermal arsenic(III) in streamwaters of the eastern Sierra Nevada.” Environ. Sci. Technol., 32(5), 657–662.
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Received: Sep 13, 2005
Accepted: Jun 14, 2006
Published online: Jan 1, 2007
Published in print: Jan 2007
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