Abstract
Arsenic is subject to microbial interactions, which support a wide range of biogeochemical transformations of elements in natural environments such as wetlands. The arsenic detoxification potential of the bacterial strains was investigated with the arsenite oxidation gene, aox genotype, which were isolated from the natural and constructed wetlands. The isolates were able to grow in the presence of 10 mM of sodium arsenite (As(III) as NaAsO2) and 1 mM of d+glucose. Phylogenetic analysis based on 16S rRNA gene sequencing indicated that these isolated strains resembled members of the genus that have arsenic-resistant systems (Acinetobacter sp., Aeromonas sp., Agrobacterium sp., Comamonas sp., Enterobacter sp., Pantoea sp., and Pseudomonas sp.) with sequence similarities of 81–98%. One bacterial isolate identified as Pseudomonas stutzeri strain GIST-BDan2 (EF429003) showed the activity of arsenite oxidation and existence of aoxB and aoxR gene, which could play an important role in arsenite oxidation to arsenate. This reaction may be considered as arsenic detoxification process. The results of a batch test showed that P. stutzeri GIST-BDan2 (EF429003) completely oxidized in 1 mM of As(III) to As(V) within 25–30 h. In this study, microbial activity was evaluated to provide a better understanding of arsenic biogeochemical cycle in both natural and constructed wetlands, where ecological niches for microorganisms could be different, with a specific focus on arsenic oxidation/reduction and detoxification.
Similar content being viewed by others
References
Ahmann, D. A., Roberts, L., Krumholz, L. R., & Morel, F. M. M. (1994). Microbe grows by reducing arsenic. Nature, 371, 750. doi:10.1038/371750a0.
Alewell, C., Paul, S., Lischid, G., Kűsel, K., & Gehre, M. (2006). Characterizing the redox status in three different forested wetlands with geochemical data. Environmental Science and Technology, 40, 7609–7615. doi:10.1021/es061018y.
Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402. doi:10.1093/nar/25.17.3389.
Barbieri, P., Galassi, G., & Galli, E. (1989). Plasmid-encoded mercury resistance in a Pseudomonas stutzeri strain that degrades o-xylene. EFMS Microbiology Ecology, 62, 375–384. doi:10.1111/j.1574-6968.1989.tb03393.x.
Batty, L. C., Atkin, L., & Manning, D. A. C. (2005). Assessment of the ecological potential of mine-water treatment wetlands using a baseline survey of macroinvertebrate communities. Environmental Pollution, 138, 412–419. doi:10.1016/j.envpol.2005.04.022.
Batty, L. C., Baker, A. J. M., & Wheeler, B. D. (2006). The effect of vegetation on porewater composition in a natural wetlands receiving acid mine drainage. Wetlands, 6, 40–48. doi:10.1672/0277-5212(2006)26[40:TEOVOP]2.0.CO;2.
Bhumbia, D. K., & Keefer, R. F. (1994). Arsenic mobilization and bioavailability in soils. In J. O. Nriagu (Ed.), Arsenic in the environment (pp. 51–82). New York: Wiley.
Burke, M. E., Gorham, E., & Pratt, D. C. (1974). Distribution of purple photosynthetic bacteria in wetlands and woodland habitats of central and northern Minnesota. Journal of Bacteriology, 117, 826–833.
Carbonell, A. A., Aarabi, M. A., DeLaune, R. D., Gambrell, R. P., & Patrick, W. H., Jr. (1998). Arsenic in wetland vegetation: availability, phytotoxicity, uptake and effects on plant growth and nutrition. The Science of the Total Environment, 217, 189–199. doi:10.1016/S0048-9697(98)00195-8.
Cervantes, C., Ji, G., Ramirez, J. L., & Silver, S. (1994). Resistance to arsenic compounds in microorganisms. FEMS Microbiology Reviews, 15, 355–367. doi:10.1111/j.1574-6976.1994.tb00145.x.
Chang, Y. H., Han, J. I., Chun, J. S., Lee, K. C., Rhee, M. S., Kim, Y. B., et al. (2002). Comamonas koreensis sp. nov., a non-motile species from wetlands in Woopo, Korea. International Journal of Systematic and Evolutionary Microbiology, 52, 377–381.
Chang, J. S., Kim, Y.-H., & Kim, K. W. (2008). The ars genotype characterization of arsenic-resistant bacteria from arsenic-contaminated gold-silver mines in the Republic of Korea. Applied Microbiology and Biotechnology, 80, 155–165. doi:10.1007/s00253-008-1524-0.
Chang, J. S., Yoon, I. H., & Kim, K. W. (2007). Isolation and ars detoxification of arsenic-oxidizing bacteria from abandoned arsenic-contaminated mines. Journal of Microbiology and Biotechnology, 17, 812–821.
D’Angelo, E. M., & Reddy, K. R. (1999). Regulators of heterotrophic microbial potentials in wetlands soils. Soil Biology and Biochemistry, 31, 815–830.
Dedysh, S. N., Panikov, N. S., Liesack, W., Grobokpf, R., Zhou, J., & Tiedje, J. M. (1998). Isolation of acidophilic methane-oxidizing bacteria from northern peat wetlands. Science, 282, 281–284.
Dunne, E. J., Reddy, R., & Clark, M. W. (2006). Biogeochemical indices of phosphorus retention and release by wetlands soils and adjacent stream sediments. Wetlands, 26, 1026–1041.
Hallberg, K. B., & Johnson, D. B. (2005). Microbiology of a wetlands ecosystem constructed to remediate mine drainage from a heavy metal mine. Science of the Total Environment, 338, 53–66.
Ibrahim, F., Halttunen, T., Tahvonen, R., & Salminen, S. (2006). Probiotic bacteria as potential detoxification tools: assessing their heavy metal binding isotherms. Canadian Journal of Microbiology, 52, 877–885.
Jackson, C. R., Langner, H. W., Donahoe-Christiansen, J., Inskeep, W. P., & McDermott, T. R. (2001). Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring. Environmental Microbiology, 3, 532–542.
Ji, G., & Silver, S. (1992a). Regulation and expression of the arsenic resistance operon from Staphylococcus aureus plasmid pl258. Journal of Bacteriology, 174, 3684–3694.
Ji, G., & Silver, S. (1992b). Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon of Staphylococcus aureus plasmid pl258. Proceedings of the National Academy of Science of the United States of America, 89, 9474–9478.
Kashyap, D. P., Botero, L. M., Franck, W. L., Hassett, D. J., & McDermott, T. R. (2006). Complex regulation of arsenite oxidation in Agrobacterium tumefaciens. Journal of Bacteriology, 188, 1081–1088.
Le, X. C., Yalcin, S., & Ma, M. (2000). Speciation of submicrogram per liter levels of arsenic in water: on site species separation integrated with sample collection. Environmental Science and Technology, 34, 2342–2347.
Lee, S. J., Lee, S. C., Choi, S. H., Chung, M. K., Rhie, H. G., & Lee, H. S. (2001). Effect of ArsA, Arsenite-specific ATPase, on inhibition of cell division in Escherichia coli. Journal of Microbiology Biotechnology, 11, 825–830.
Lee, Y. J., Romanek, C. S., Mills, G. L., Davis, R. C., Whitman, W. B., & Wiegel, J. G. (2006). Gracilibacter thermotolerans gen. nov., sp. nov., an anaerobic, thermotolerant bacterium from a constructed wetlands receiving acid sulfate water. International Journal of Systematic and Evolutional Microbiology, 56, 2089–2093.
Li, J., & Gu, J. D. (2007). Complete degradation of dimethyl isophthalate requires the biochemical cooperation between Klebsiella oxytoca Sc and Methylobacterium mesophilicum Sr isolated from wetlands sediment. Science of the Total Environment, 380, 181–187.
Mitchell, L. K., & Karathanasis, A. D. (1995). Treatment of metal–chloride-enriched wastewater by simulate constructed wetlands. Environmental Geochemistry and Health, 17, 119–126.
Mukhopadhyay, R., Rosen, B. P., Phung, L. T., & Silver, S. (2002). Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiology Review, 26, 311–325.
Muller, D., Liévremont, D., Simeonova, D. D., Hubert, J.-C., & Lett, M.-C. (2003). Arsenite oxidase aox genes from a metal-resistant β-proteobacterium. Journal of Bacteriology, 185, 135–141.
Oremland, R. S., Kulp, T. R., Switzer, B. J., Hoeft, S. E., Baesman, S., Milluer, L. G., et al. (2005). A microbial arsenic cycle in a salt-saturated extreme environment. Science, 308, 1305–1308.
Oremland, R. S., & Stolz, J. F. (2003). The ecology of arsenic. Science, 300, 939–944.
Oremland, R. S., Tolz, J. F., & Hollibaugh, J. T. (2004). The microbial arsenic cycle in MonoLake, California. FEMS Microbiology Ecology, 48, 15–27.
Park, N. O., Kim, J. H., & Cho, J. W. (2008). Organic matter, anion and metal wastewater treatment in Damyang surface-flow constructed wetlands in Korea. Ecological Engineering, 32, 68–71.
Sambrook, J., & Russel, D. W. (2001). Molecular cloning: a laboratory manual (3rd edn.). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Santini, J. M., Sly, L. I., Schnagl, R. D., & Macy, J. M. (2000). A new chemolithotrophic arsenite-oxidizing bacterium isolated from a goldmine: phylogenetic, physiological and preliminary biochemical studies. Applied and Environmental Microbiology, 66, 92–97.
Silver, S., & Phung, L. T. (2005). Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Applied and Environmental Microbiology, 71, 599–608.
Sima, J., Diáková, K., & Holcová, V. (2007). Redox processes of sulfur and manganese in a constructed wetlands. Chemistry & Biodiversity, 4, 2900–2912.
Ure, A. M. (1995). Methods of analysis for heavy metals in soils. In B. J. Alloway (Ed.), Heavy metals in soils (pp. 55–68). London: Glasgow.
Vymazal, J., Švehla, J., Kröpfelová, L., & Chrastný, V. (2007). Trace metals in Ragmites australis and Phalaris arundinacea growing in constructed and natural wetlands. Science of the Total Environment, 380, 154–162.
Wang, J. P., Qi, L., Moore, M. R., & Ng, J. C. (2002). A review of animal models for the study of arsenic carcinogenesis. Toxicology Letters, 133, 17–31.
Webb, J. S., McGinness, S., & Lappin-Scott, H. M. (1998). Metal removal by sulphate- reducing bacteria from natural and constructed wetlands. Journal of Applied Microbiology, 84, 240–248.
Weber, K. A., Urrutia, M. M., Churchill, P. F., Kukkadapu, R. K., & Roden, E. E. (2006). Anaerobic redox cycling of iron freshwater sediment microorganisms. Environmental Microbiology, 8, 100–113.
Weiss, J. V., Emerson, D., & Patrick Megonigal, L. (2004). Geochemical control of microbial Fe(III) reduction potential in wetlands: comparison of the rhizosphere to non-rhizosphere soil. FEMS Microbiology Ecology, 48, 89–100.
White, A. K., & Metcalf, W. W. (2004). Two C-P lyase operons in Pseudomonas stutzeri and their roles in the oxidation of phosphonates, phosphite, and hypophosphite. Journal of Bacteriology, 186, 4730–4739.
Yoon, I. H., Chang, J. S., Lee, J. H., & Kim, K. W. (2008). Arsenite oxidation by Alcaligenes sp. strain RS-19 isolated from arsenic-contaminated mine area in South Korea. Environmental Geochemistry and Health, 31(10), 9–117.
Zedler, J. B., & Kercher, S. (2005). Wetlands resources: status, trends, ecosystem services, and restorability. Annual Review Environment and Resources, 30, 39–74.
Acknowledgments
This work was supported by the Korea Science and Engineering Foundation (KOSEF) through the National Research Laboratory program funded by the Ministry of Science and Technology (no. M10300000298-06J0000-29810). Ji-Hoon Lee was supported by the Korea Research Foundation Grant funded by the Korean Government (MOEHRD) (KRF-2007-357-D00141).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chang, JS., Yoon, IH., Lee, JH. et al. Arsenic detoxification potential of aox genes in arsenite-oxidizing bacteria isolated from natural and constructed wetlands in the Republic of Korea. Environ Geochem Health 32, 95–105 (2010). https://doi.org/10.1007/s10653-009-9268-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10653-009-9268-z