DOI QR코드

DOI QR Code

Characteristics of Dissimilatory Arsenate-reducing Bacteria

이화형비산염환원균의 특성

  • Chang, Young-Cheol (Biosystem Course, Division of Applied Sciences, Muroran Institute of Technology) ;
  • Takamizawa, Kazuhiro (Department of Applied Life Science, Faculty of Applied Biological Sciences, Gifu University) ;
  • Cho, Hoon (Department of Polymer Science & Engineering, Chosun University) ;
  • Kikuchi, Shintaro (Biosystem Course, Division of Applied Sciences, Muroran Institute of Technology)
  • Received : 2012.04.11
  • Accepted : 2012.04.24
  • Published : 2012.04.30

Abstract

Although, microbial arsenic mobilization by dissimilatory arsenate-reducing bacteria (DARB) and the practical use to the removal technology of arsenic from contaminated soil are expected, most previous research mainly has been focused on the geochemical circulation of arsenic. Therefore, in this review we summarized the previously reported DARB to grasp the characteristic for bioremediation of arsenic. Evidence of microbial growth on arsenate is presented based on isolate analyses, after which a summary of the physiology of the following arsenate-respiring bacteria is provided: Chrysiogenes arsenatis strain BAL-$1^T$, Sulfurospirillum barnesii, Desulfotomaculum strain Ben-RB, Desulfotomaculum auripigmentum strains OREX-4, GFAJ-1, Bacillus sp., Desulfitobacterium hafniense DCB-$2^T$, strain SES-3, Citrobacter sp. (TSA-1 and NC-1), Sulfurospirillum arsenophilum sp. nov., Shewanella sp., Chrysiogenes arsenatis BAL-$1^T$, Deferribacter desulfuricans. Among the DARB, Citrobacter sp. NC-1 is superior to other dissimilatory arsenate-reducing bacteria with respect to arsenate reduction, particularly at high concentrations as high as 60 mM. A gram-negative anaerobic bacterium, Citrobacter sp. NC-1, which was isolated from arsenic contaminated soil, can grow on glucose as an electron donor and arsenate as an electron acceptor. Strain NC-1 rapidly reduced arsenate at 5 mM to arsenite with concomitant cell growth, indicating that arsenate can act as the terminal electron acceptor for anaerobic respiration (dissimilatory arsenate reduction). To characterize the reductase systems in strain NC-1, arsenate and nitrate reduction activities were investigated with 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. Tungstate, which is a typical inhibitory antagonist of molybdenum containing dissimilatory reductases, strongly inhibited the reduction of arsenate and nitrate in anaerobic growth cultures. These results suggest that strain NC-1 catalyzes the reduction of arsenate and nitrate by distinct terminal reductases containing a molybdenum cofactor. This may be advantageous during bioremediation processes where both contaminants are present. Moreover, a brief explanation of arsenic extraction from a model soil artificially contaminated with As (V) using a novel DARB (Citrobacter sp. NC-1) is given in this article. We conclude with a discussion of the importance of microbial arsenate reduction in the environment. The successful application and use of DARB should facilitate the effective bioremediation of arsenic contaminated sites.

Keywords

References

  1. Pontius F., K. G, Brown, and C. J. Chen (1994) Health implications of arsenic in drinking water. J. Am. Water Works Assoc. 86: 52-63.
  2. Alam, M. G. M., S. Tokunaga, and T. Maekawa (2001) Extraction of arsenic in a synthetic arsenic-contaminated soil using phosphate. Chemosphere 43: 1035-1041. https://doi.org/10.1016/S0045-6535(00)00205-8
  3. Macy, J. M., K. Nunan, K. D. Hagen, D. R. Dixon, P. J. Harbour, M. Cahill, and L. I. Sly (1996) Chrysiogenes arsenatis gen. nov., sp. nov., a new arsenate-respiring bacterium isolated from gold mine wastewater. Int. J. Syst. Bacteriol. 46: 1153-1157. https://doi.org/10.1099/00207713-46-4-1153
  4. Gates, A. J., R. O. Hughes, S. R. Sharp, P. D. Millington, A. Nilavongse, J. A. Cole, E. R. Leach, B. Jepson, D. J. Richardson, and C. S. Butler (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. https://doi.org/10.1016/S0378-1097(03)00122-8
  5. Oremland, R. S. and J. F. Stolz (2003) The ecology of arsenic. Science. 300: 939-944. https://doi.org/10.1126/science.1081903
  6. Ahmann, D., A. L. Roberts, L. R. Krumholtz, and F. M. M. Morel (1994) Microbe grows by reducing arsenic. Nature. 371: 750-751. https://doi.org/10.1038/371750a0
  7. Rittle, K. A., J. I. Drever, and P. J. S. Colbeerg (1995) Precipitation of arsenic during sulfate reduction. Geomicrobiol. J. 13: 1-12. https://doi.org/10.1080/01490459509378000
  8. Laverman, A. M., J. S. Blum, J. K. Schaefer, E. J. P. Phillips, D. R. Lovley, and R. S. Oremland (1995) Growth of strain SES-3 with arsenate and other diverse electron acceptors. Appl. Environ. Microbiol. 61: 3556-3561.
  9. Newman, D. K., E. K. Kennedy, J. D. Coates, D. Ahmann, D. J. Ellis, and D. R. Morel (1997) Dissimilatory arsenate and sulfate reduction in Desulfotomaculum auripigmentum sp. nov. Arch. Microbiol. 168: 380-388. https://doi.org/10.1007/s002030050512
  10. Oremland, R. S., J. S. Blum, C. W. Culbertson, P. T. Visscher, L. G. Miller, P. Dowdle, and F. E. Strohmaier (1994) Isolation, growth, and metabolism of an obligately anaerobic, selenate-respiring bacterium, strain SES-3. Appl. Environ. Microbiol. 60: 3011-3019.
  11. Liu, A., E. Garcia-Doninguez, E. D. Rhine, and L. Y. Young (2004) A novel arsenate respiring isolate that can utilize aromatic substrates. FEMS Microbiol. Ecol. 48: 323-332. https://doi.org/10.1016/j.femsec.2004.02.008
  12. Manning, B. A. and S. Goldberg (1997) Arsenic (III) and arsenic (V) adsorption on three California soils. Soil Sci. 162: 886-895. https://doi.org/10.1097/00010694-199712000-00004
  13. Newman, D. K., T. J. Beveridge, and F. M. M. Morel (1997) Precipitation of arsenic trisulfide by Desulfotomaculum auripigmentum. Appl. Environ. Microbiol. 63: 2022-2028.
  14. Kraft, T. and J. M. Macy (1998) Purification and characterization of the respiratory arsenate reductase of Chrysiogenes arsenatis. Eur. J. Biochem. 255: 647-653. https://doi.org/10.1046/j.1432-1327.1998.2550647.x
  15. Chauret, C. and R. Knowles (1991) Effect of tungsten on nitrate and nitrite reductases in Azospirillum brasilense Sp7. Can. J. Microbiol. 37: 744-750. https://doi.org/10.1139/m91-128
  16. Kashiwa, M., S. Nishimoto, K. Takahashi, M. Ike, and M. Fujita (2000) Factors affecting soluble selenium removal by a selenate-reducing bacterium Bacillus sp. SF-1. J. Biosci. Bioeng. 89: 528-533. https://doi.org/10.1016/S1389-1723(00)80051-1
  17. Ahmann, D., L. R. Krumholz, H. F. Hemond, D. R. Lovley, and F. M. M. Morel (1997) Microbial mobilization of arsenic from sediments of the Aberjona watershed. Environ. Sci. Technol. 31: 2923-2930. https://doi.org/10.1021/es970124k
  18. Herbel, M. J., J. S. Blum, S. E. Hoeft, S. M. Cohen, L. L. Arnold, J. Lisak, J. F. Stolz, and R. S. Oremland (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. https://doi.org/10.1111/j.1574-6941.2002.tb00966.x
  19. Yamamura, S., N. Yamamoto, M. Ike, and M. Fujita (2005) Arsenic extraction from solid phase using a dissimilatory arsenate-reducing bacterium. J. Biosci. Bioeng. 100: 219-222. https://doi.org/10.1263/jbb.100.219
  20. Gihring, T. M. and J. F. Banfield (2001) Arsenite oxidation and arsenate respiration by a new Thermus isolate. FEMS Microbiol. Lett. 204: 335-340. https://doi.org/10.1111/j.1574-6968.2001.tb10907.x
  21. Takai, K., H. Kobayashi, K. H. Nealson, and K. Horikoshi (2003) Deferribacter desulfuricans sp. nov., a novel sulfer-, nitrate-and arsenate-reducing thermophile isolated from a deepsea hydrothermal vent. Int. J. Syst. Evol. Microbiol. 53: 839-846. https://doi.org/10.1099/ijs.0.02479-0
  22. Blum, J. S., A. B. Bindi, J. Buzzelli, J. F. Stolz, and R. S. Oremland (1998) Bacillus arsenicoselenatis, sp. nov., Bacillus selenitireducens, sp.nov.: two haloalkaliphiles from Mono lake, California that respire oxyanions of selenium and arsenic. Arch. Microbiol. 171: 19-30. https://doi.org/10.1007/s002030050673
  23. Afkar, E., J. Lisak, C. Saltikov, P. Basu, R. S. Oremland, and J. F. Stolz (2003) The respiratory arsenate reductase Bacillus selenitireducens strain MLAS10. FEMS Microbiol. Lett. 226: 107-112. https://doi.org/10.1016/S0378-1097(03)00609-8
  24. Santini, J. M., J. F. Stolz, and J. M. Macy (2002) Isolation of a new arsenate-respiring bacterium-physiological and phylogenetic studies. Geomicrobiol. J. 19: 41-52. https://doi.org/10.1080/014904502317246156
  25. Fujita, M., M. Ike, S. Nishimoto, K. Takahashi, and M. Kashiwa (1997) Isolation and characterization of a novel selenate-reducing bacterium, Bacillus sp. SF-1. J. Ferment. Bioeng. 83: 517-522. https://doi.org/10.1016/S0922-338X(97)81130-0
  26. Yamamura, S., M. Ike, and M. Fujita (2003) Dissimilatory arsenate reduction by a facultative anaerobe, Bacillus sp. strain SF-1. J. Biosci. Bioeng. 96: 454-460. https://doi.org/10.1016/S1389-1723(03)70131-5
  27. Niggemyer, A., S. Spring, E. Stackebrandt, and R. F. Rosenzweig (2001) Isolation and characterization of a novel As (V)-reducing bacterium: implication for arsenic mobilization and the genus Desulfitobacterium. Appl. Environ. Microbiol. 67: 5568-5580. https://doi.org/10.1128/AEM.67.12.5568-5580.2001
  28. Bouchard, B., R. Beaudet, R. Villemur, G. Mcsween, F. Lepine, and J. G. Bisaillon (1996) Isolation and characterization of Desulfitobacterium frapperi sp. nov., an anaerobic bacterium which reductively dechlorinates pentachlorophenol to 3-chlorophenol. Int. J. Syst. Bacteriol. 46: 1010-1015. https://doi.org/10.1099/00207713-46-4-1010
  29. Christiansen, N. and B. K. Ahring (1996) Desulfitobacterium hafniense sp. nov., an anaerobic, reductively dechlorinating bacterium. Int. J. Syst. Bacteriol. 46: 442-448. https://doi.org/10.1099/00207713-46-2-442
  30. Stackebrandt, E., P. Schumann, E. Schuler, and H. Hippe (2003) Reclassification of Desulfotomaculum auripigmentum as Desulfosporosinus auripigmenti corrig., comb. nov. Int. J. Syst. Evol. Microbiol. 53: 1439-1443. https://doi.org/10.1099/ijs.0.02526-0
  31. Chang, Y. C., A. Nawata, K. Jung, and S. Kikuchi, 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
  32. Saltikov, C. W., A. Cifuentes, K. Venkateswaran, and D. K. Newman (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. https://doi.org/10.1128/AEM.69.5.2800-2809.2003
  33. Felisa,W. S., J. S. Blum, T. R. Kulp, G. W. Gordon, S. E. Hoeft, J. Pett-Ridge, J. F. Stolz, S. M. Webb, P. K. Weber, P. C. W. Davies, A. D. Anbar, and R. S. Oremland (2011) A bacterium that can grow by using arsenic instead of phosphorus. Science. 332, 1163-1166. https://doi.org/10.1126/science.1197258
  34. Hoeft, S. E., T. R. Kulp, J. F. Stolz, J. T. Hollibaugh, and R. S. Oremland (2004) Dissimilatory arsenate reduction with sulfide as electron donor: experiments with Mono lake water and isolation of strain MLMS-1, a chemoautotorophic arsenate respirer. Appl. Environ. Microbiol. 70: 2741-2747. https://doi.org/10.1128/AEM.70.5.2741-2747.2004
  35. Macy, J. M., J. M. Santini, B. V. Pauling, A. H. O'Neill, and L. I. Sly (2000) Two new arsenate/sulfate-reducing bacteria: mechanisms of arsenate reduction. Arch. Microbiol. 173: 49-57. https://doi.org/10.1007/s002030050007
  36. Stolz, J. F., D. J. Ellis, J. S. Blum, D. Ahmann, D. R. Lovley, and R. S. Oremland (1999) Sulfurosirillum barnesii sp. nov. and Sulfurospirillum arsenophilum sp. nov., new members of the Sulfurospirillum clade of the ${\varepsilon}$ proteobacteria. Int. J. Syst. Bacteriol. 49: 1177-1180. https://doi.org/10.1099/00207713-49-3-1177
  37. Oremland, R. S., J. S. Blum, A. B. Bindi, P. R. Dowdle, M. Herbel, and J. F. Stolz (1999) Simultaneous reduction of nitrate and selenate by cell suspensions of selenium respiring bacteria. Appl. Environ. Microbiol. 65: 4385-4392.
  38. Zobrist, J., P. R. Dowdle, J. A. Davis, and R. S. Oremland (2000) Mobilization of arsenite by dissimilatory reduction of adsorbed arsenate. Environ. Sci. Technol. 34: 4747-4753. https://doi.org/10.1021/es001068h
  39. Bagla, P. and J. Kaiser (1996) India's spreading health crisis draws global arsenic experts. Science. 274: 174-175. https://doi.org/10.1126/science.274.5285.174
  40. Langner, H. W. and W. P. Inskeep (2000) Microbial reduction of arsenate in the presence of ferrihydrite. Environ. Sci. Technol. 34: 3131-3136. https://doi.org/10.1021/es991414z
  41. Prins, R. A., W. Cline-Theil, A. Malestein, and G. H. M. Counotte (1980) Inhibition of nitrate reduction in some rumen bacteria by tungstate. Appl. Environ. Microbiol. 40: 163-165.
  42. Dowdle, P. R., A. M. Laverman, and R. S. Oremland (1996) Bacterial dissimilatory reduction of arsenate (V) to arsenic (III) in anoxic sediments. Appl. Environ. Microbiol. 62: 1664-1669.
  43. Lovley, D. R. and J. D. Coates (1997) Bioremediation of metal contamination. Curr. Opin. Biotechnol. 8: 285-289. https://doi.org/10.1016/S0958-1669(97)80005-5