Abstract
A Gram-negative anaerobic bacterium, Citrobacter sp. NC-1, was isolated from soil contaminated with arsenic at levels as high as 5,000 mg As kg−1. Strain NC-1 completely reduced 20 mM arsenate within 24 h and exhibited arsenate-reducing activity at concentrations as high as 60 mM. These results indicate that strain NC-1 is superior to other dissimilatory arsenate-reducing bacteria with respect to arsenate reduction, particularly at high concentrations. Strain NC-1 was also able to effectively extract arsenic from contaminated soils via the reduction of solid-phase arsenate to arsenite, which is much less adsorptive than arsenate. To characterize the reductase systems in strain NC-1, arsenate and nitrate reduction activities were investigated using washed-cell suspensions and crude cell extracts from cells grown on arsenate or nitrate. These reductase activities were induced individually by the two electron acceptors. This may be advantageous during bioremediation processes in which both contaminants are present.
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References
Ahmann D, Krumholz LR, Hemond HF, Lovley DR, Morel FMM (1997) Microbial mobilization of arsenic from sediments of the Aberjona watershed. Environ Sci Technol 31:2923–2930
Ahmann D, Roberts AL, Krumholtz LR, Morel FMM (1994) Microbe grows by reducing arsenic. Nature 371:750
Alam MG, Tokunaga S, Maekawa T (2001) Extraction of arsenic in a synthetic arsenic-contaminated soil using phosphate. Chemosphere 43:1035–1041
Bagla P, Kaiser J (1996) India’s spreading health crisis draws global arsenic experts. Science 274:174–175
Chang YC, Shintaro K (2010) Isolation and characterization of arsenate-reducing bacteria from arsenic-contaminated site in Japan. In: 2nd proceedings of studies of environmental issues in the Asian mega-cities, Seoul, Korea. pp 213–221
Butcher BG, Deane SM, Rawlings DE (2000) The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl Environ Microbiol 66:1826–1833
Chauret C, Knowles R (1991) Effect of tungstate on nitrate and nitrite reductases in Azospirillum brasilense Sp7. Can J Microbiol 37:744–750
Dowdle PR, Laverman AM, Oremland RS (1996) Bacterial dissimilatory reduction of arsenic(V) to arsenic(III) in anoxic sediments. Appl Environ Microbiol 62:1664–1669
Fujita M, Ike M, Nishimoto S, Takahashi K, Kashiwa M (1997) Isolation and characterization of a novel selenate-reducing bacterium, Bacillus sp. SF-1. J Ferment Bioeng 83:517–522
Gates AJ, Hughes RO, Sharp SR, Millington PD, Nilavongse A, Cole JA, Leach ER, Jepson B, Richardson DJ, Butler CS (2003) Properties of the periplasmic nitrate reductases from Paracoccus pantotrophus and Escherichia coli after growth in tungsten supplemented media. FEMS Microbiol Lett 220:261–269
Herbel MJ, Blum JS, Hoeft SE, Cohen SM, Arnold LL, Lisak J, Stolz JF, Oremland RS (2002) Dissimilatory arsenate reductase activity and arsenate-respiring bacteria in bovine rumen fluid, hamster feces, and the termite hindgut. FEMS Microbiol Ecol 41:59–67
Jareonmit P, Kannika S, Michael JS (2010) Structure and diversity of arsenic-resistant bacteria in an old tin mine area of Thailand. J Microbiol Biotechnol 20:169–178
Kashiwa M, Nishimoto S, Takahashi K, Ike M, Fujita M (2000) Factors affecting soluble selenium removal by a selenate-reducing bacterium Bacillus sp. SF-1. J Biosci Bioeng 89:528–533
Kraft T, Macy JM (1998) Purification and characterization of the respiratory arsenate reductase of Chrysiogenes arsenatis. Eur J Biochem 255:647–653
Langner HW, Inskeep WP (2000) Microbial reduction of arsenate in the presence of ferrihydrite. Environ Sci Technol 34:3131–3136
Laverman AM, Blum JS, Schaefer JK, Phillips EJP, Lovley DR, Oremland RS (1995) Growth of strain SES-3 with arsenate and other diverse electron acceptors. Appl Environ Microbiol 61:3556–3561
Lovley DR, Coates JD (1997) Bioremediation of metal contamination. Curr Opin Biotechnol 8:285–289
Lovley DR, Phillips EJP (1986) Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol 51:683–689
Macur RE, Wheeler JT, Mcdermott TR, Inskeep WP (2001) Microbial populations associated with the reduction and enhanced mobilization of arsenic in mine tailings. Environ Sci Technol 35:3676–3682
Manning BA, Goldberg S (1997) Arsenic(III) and arsenic(V) adsorption on three California soils. Soil Sci 162:886–895
Newman DK, Beveridge TJ, Morel FMM (1997) Precipitation of arsenic trisulfide by Desulfotomaculum auripigmentum. Appl Environ Microbiol 63:2022–2028
Newman DK, Kennedy EK, Coates JD, Ahmann D, Ellis DJ, Lovley DR, Morel FMM (1997) Dissimilatory arsenate and sulfate reduction in Desulfotomaculum auripigmentum sp. nov. Arch Microbiol 168:380–388
Oremland RS, Blum JS, Bindi AB, Dowdle PR, Herbel M, Stolz JF (1999) Simultaneous reduction of nitrate and selenate by cell suspensions of selenium respiring bacteria. Appl Environ Microbiol 65:4385–4392
Oremland RS, Stolz JF (2003) The ecology of arsenic. Science 300:939–944
Pontius F, Brown KG, Chen CJ (1994) Health implications of arsenic in drinking water. J Am Water Works Assoc 86:52–63
Prins RA, Cline-Theil W, Malestein A, Counotte GHM (1980) Inhibition of nitrate reduction in some rumen bacteria by tungstate. Appl Environ Microbiol 40:163–165
Rittle KA, Drever JI, Colbeerg PJS (1995) Precipitation of arsenic during sulfate reduction. Geomicrobiol J 13:1–12
Roberts LC, Hug SJ, Ruettimann T, Billah MM, Khan AW, Rahman MT (2004) Arsenic removal with iron(II) and iron(III) in waters with high silicate and phosphate concentrations. Environ Sci Technol 38:307–315
Sakata M (1987) Relationship between adsorption of arsenic(III) and boron by soil and soil properties. Environ Sci Technol 21:1126–1130
Saltikov CW, Cifuentes A, Venkateswaran K, Newman DK (2003) The ars detoxification system is advantageous but not required for As(V) respiration by the genetically tractable Shewanella species strain ANA-3. Appl Environ Microbiol 69:2800–2809
Saltikov CW, Olson BH (2002) Homology of Escherichia coli R773 arsA, arsB, and arsC genes in arsenic-resistant bacteria isolated from raw sewage and arsenic-enriched creek waters. Appl Environ Microbiol 68:280–288
Smith E, Naidu R, Alston AM (1999) Chemistry of arsenic in soils: I. Sorption of arsenate and arsenite by for Australian soils. J Environ Qual 28:1719–1726
Soda S, Kanzaki M, Yamamura S, Kashiwa M, Fujita M, Ike M (2009) Slurry bioreactor modeling using a dissimilatory arsenate-reducing bacterium for remediation of arsenic-contaminated soil. J Biosci Bioeng 107:130–137
Stolz JF, Gugliuzza T, Blum JS, Oremland R, Murillo FM (1997) Differential cytochrome content and reductase activity in Geospirillum barnesii strain SeS3. Arch Microbiol 167:1–5
Tamaki S, Frankenberger WT (1992) Environmental biochemistry of arsenic. Rev Environ Contam Toxicol 124:79–110
Tokunaga S, Hakuta T (2002) Acid washing and stabilization of an artificial arsenic contaminated soil. Chemosphere 46:31–38
Yamamura S, Ike M, Fujita M (2003) Dissimilatory arsenate reduction by a facultative anaerobe, Bacillus sp. strain SF-1. J Biosci Bioeng 96:454–460
Yamamura S, Yamamoto N, Ike M, Fujita M (2005) Arsenic extraction from solid phase using a dissimilatory arsenate-reducing bacterium. J Biosci Bioeng 100:219–222
Zobrist J, Dowdle PR, Davis JA, Oremland RS (2000) Mobilization of arsenite by dissimilatory reduction of adsorbed arsenate. Environ Sci Technol 34:4747–4753
Acknowledgments
We thank Dr. Michihiko Ike, University of Osaka, for his kind cooperation in collection of the samples. The authors also thank Dr. Tadashi Toyama, University of Yamanashi, for technical support with the analysis of arsenate. This work was partly supported by a grant (Adaptable and Seamless Technology Transfer Program through Target-driven R&D, AS211Z00600E) from the Japan Science and Technology Agency.
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Fig. 1. Phylogenic tree based on comparison of the 16S rRNA gene sequence. The phylogenic tree was generated using the neighbor-joining method. Bootstrap values shown are based on 100 replications. Scale bar represents 0.005% sequence difference. Supplementary material 2 (DOC 42 kb)
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Chang, Y.C., Nawata, A., Jung, K. et al. Isolation and characterization of an arsenate-reducing bacterium and its application for arsenic extraction from contaminated soil. J Ind Microbiol Biotechnol 39, 37–44 (2012). https://doi.org/10.1007/s10295-011-0996-6
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DOI: https://doi.org/10.1007/s10295-011-0996-6