Microbial perchlorate reduction: Rocket-fuelled metabolism

Nature Reviews Microbiology

Volumn 2, Issue 7, 2004, Pages 569-580

  Coates, John D ^a   Achenbach, Laurie A ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SOUTHERN ILLINOIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANION; CHLORIDE; ISOTOPE; PERCHLORATE; RIBOSOME RNA; RNA 16S; BACTERIAL DNA; PERCHLORIC ACID;

BACTERIAL GENETICS; BACTERIAL METABOLISM; BACTERIUM IDENTIFICATION; BIOCHEMISTRY; BIOREMEDIATION; CHEMICAL REACTION; DECHLOROMONAS AROMATICA; ENDOCRINE DISEASE; GENE SEQUENCE; GRAM NEGATIVE BACTERIUM; IMMUNOLOGY; MICROBIAL GENETICS; MOLECULAR BIOLOGY; NONHUMAN; OXIDATION REDUCTION REACTION; PHYLOGENY; PRIORITY JOURNAL; REVIEW; SOLUBILITY; UNITED STATES; WATER CONTAMINATION; GENETICS; METABOLISM; PROTEOBACTERIA; WATER POLLUTANT;

BACTERIA (MICROORGANISMS); DECHLOROMONAS; DECHLOROMONAS AROMATICA; HESPERIS; NEGIBACTERIA;

BIODEGRADATION, ENVIRONMENTAL; DNA, BACTERIAL; OXIDATION-REDUCTION; PERCHLORIC ACID; PROTEOBACTERIA; RNA, RIBOSOMAL, 16S; WATER POLLUTANTS, CHEMICAL;

EID: 3142726522     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro926     Document Type: Review

References (95)

1. Waldman, P. Pentagon hid pollution report lawmakers say. Wall Street Journal (New York, 19 May 2003).
2. Renner, R. Perchlorate regulation faces further delay. Environ. Sci. Technol. 37, 166A-167A (2003).
3. Hogue, C. Rocket-fueled river. Chem. Eng. News 81, 37-46 (2003).
4. Urbansky, E. T. Quantitation of perchlorate ion: practices and advances applied to the analysis of common matrices. Crit. Rev. Anal. Chem. 30, 311-343 (2000).
5. Orris, G. J., Harvey, G. J., Tsui, D. T. & Eldrige, J. E. Open-File Report 03-314 US Geological Survey, Tucson, Arizona (2003).
6. Collette, T. W. et al. Analysis of hydroponic fertilizer matrixes for perchlorate: comparison of analytical techniques. Analyst 128, 88-97 (2003).
7. Christen, K. EPA perchlorate decision takes many by surprise. Envirion. Sci. Technol. 37, 347A-348A (2003).
8. Motzer, W. E, Perchlorate: problems, detection, and solutions. Environ. Forensics 2, 301-311 (2001).
9. Kirk, A. B., Smith, E. E., Tian, K., Anderson, T. A. & Dasgupta, P. K. Perchlorate in milk. Environ. Sci. Technol. 37, 4979-4981 (2003).
10. Stanbury, J. B. & Wyngaarden, J. B. Effect of perchlorate on the human thyroid gland. Metabolism 1, 533-539 (1952).
11. Wolff, J. Perchlorate and the thyroid gland. Pharmacol. Rev. 50, 89-105 (1998).
12. Clark, J. J. J. in Perchlorate in the Environment (ed, Urbansky, E. T.) 15-30 (Kluwer Academic/Plenum, New York, 2000).
13. Howdeshell, K. L. A model of the development of the brain as a construct of the thyroid system. Environ. Health Perspect. 110, 337-348 (2002).
14. Porterfield, S. P. Vulnerabilities of the developing brain to thyroid abnormalities: environmental insults to the thyroid system. Environ. Health Perspect. 102, 125-130 (1994).
15. Haddow, J. E. et al. Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N. Engl. J. Med. 341, 549-555 (1999).
16. Renner, R. Perchlorate-tainted wells spur government action. Environ. Sci. Technol. 32, 210A (1998).
17. US Environmental Protection Agency. Drinking water contaminant candidate list Doc No. EPA/600/F-98/002. (Washington DC, 1998).
18. Urbansky, E. T. Perchlorate chemistry: implications for analysis and remediation. Bioremed. J. 2, 81-95 (1998).
19. Urbansky, E. T. Perchlorate as an environmental contaminant. Environ. Sci. Pollut. Res. 9, 187-192 (2002).
20. Wallace, W., Ward, T., Breen, A. & Attaway H. Identification of an anaerobic bacterium which reduces perchlorate and chlorate as Wolinella succinogenes. J. Ind. Microbiol. 16, 68-72 (1996).
21. Ericksen, G. E. The Chilean nitrate deposits. Am. Sci. 71, 366-374 (1983).
22. Schilt, A. A. Perchloric Acid and Perchlorates (The G. Fredrick Smith Chemical Comany, Ohio, 1979).
23. Urbansky, E. T., Brown, S. K., Magnusson, M. L. & Kelty, C. A. Perchlorate levels in samples of sodium nitrate fertilizer derived from Chilean caliche. Environ. Pollut. 112, 299-302 (2001).
24. -. Environ. Sci. Technol. 36, 2783-2788 (2002).
25. Susarla, S., Bacchus, T., Harvey, G. J. & McCutcheon, S. C. Phytotransformations of perchlorate contaminated waters. Environ. Technol. 21, 1055-1065 (2000).
26. Ellington, J. J. et al. Determination of perchlorate in tobacco plants and tobacco products. Environ. Sci. Technol. 35, 3213-3218 (2001).
27. Urbansky, E. T. in Chemistry and Technology of Explosives 602-620 (Pergamon Press, Oxford, 1988).
28. Roote, D. S. Technology status report perchlorate treatment technologies first edition, Doc No. DAAE30-98-C-1050 (Ground-Water Remediation Technologies Analysis Center, Pittsburgh, 2001).
29. Urbansky, E. T. & Brown, S. K. Perchlorate retention and mobility in soils. J. Environ. Monit. 5, 455-462 (2003).
30. Xu, J., Song, Y., Min, B., Steinberg, L. & Logan, B. E. Microbial degradation of perchlorate: principles and applications. Environ. Eng. Sci. 20, 405-422 (2003).
31. Aslander, A. Experiments on the eradication of Canada Thistle, Cirsium arvense, with chlorates and other herbicides. J. Agric. Res. 36, 915 (1928).
32. Coates, J. D., Michaelidou, U., O'Connor, S. M., Bruce, R. A. & Achenbach, L. A. in Perchlorate in the Environment (ed. Urbansky, E. T.) 257-270 (Kluwer Academic/Plenum, New York, 2000).
33. Bryan, E. H. & Rohlich, G. A. Biological reduction of sodium chlorate as applied to measurement of sewage BOD. Sewage Ind. Waste 26, 1315-1324 (1954).
34. Bryan, E. H. Application of the chlorate BOD procedure to routine measurement of wastewater strength. J. Wat. Pollut. Cont. Fed. 38, 1350-1362 (1966).
35. Hackenthal, E., Mannheim, W., Hackenthal, R. & Becher, R. Die reduktion von perchlorat durch bakterien. I. Untersucungen an intaken zellen. Biochem. Pharmacol. 13, 195-206 (1964).
36. Hackenthal, E. Die reduktion von perchlorat durch bacterien. II. Die identitat der nitratreduktase und des perchlorat reduzierenden enzyms aus B. cereus. Biochem. Pharm. 14, 1313-1324 (1965).
37. de Groot, G. N. & Stouthamer, A. H. Regulation of reductase formation in Proteus mirabilis. I. Formation of reductases and enzymes of the formic hydrogenlyase complex in the wild type and in chlorate resistant mutants. Arch. Microbiol. 66, 220-233 (1969).
38. Roldan, M. D., Reyes, F., Moreno-Vivian, C. & Castillo, F. Chlorate and nitrate reduction in the phototrophic bacteria Rhodobacter capsulatus and Rhodobacter sphaeroides. Curr. Microbiol. 29, 241-245 (1994).
39. Stewart, V. Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol. Pev. 52, 190-232 (1988).
40. Neidhardt, F. C. et al. (eds) Escherichia coli and Salmonella - Cellular and Molecular Biology (ASM Press, Washington DC, 1996).
41. Coates, J. D. et al. The ubiquity and diversity of dissimilatory (per)chlorate-reducing bacteria. Appl. Environ. Microbiol, 65, 5234-5241 (1999).
42. Bruce, R. A., Achenbach, L. A. & Coates, J. D. Reduction of (per)chlorate by a novel organism isolated from a paper mill waste. Environ. Microbiol. 1, 319-331 (1999).
43. Michaelidou, U., Achenbach, L. A. & Coates, J. D. in Perchlorate in the Environment (ed. Urbansky, E. T.) 271-283 (Kluwer Academic/Plenum, New York, 2000).
44. Romanenko, V. I., Korenkov, V. N. & Kuznetsov, S. I. Bacterial decomposition of ammonium perchlorate. Mikrobiologiya 45, 204-209 (1976).
45. Stepanyuk, V. et al. New species of the Acinetobacter genus Acinetobacter thermotoleranticus sp. nov. Mikrobiologiya 61, 347-356 (1992).
46. Malmqvist A. et al. Ideonella dechloratans gen. nov., sp. nov., a new bacterium capable of growing anaerobically with chlorate as an electron acceptor. System. Appl. Microbiol. 17, 58-64 (1994).
47. Rikken, G., Kroon, A. & van Ginkel, C. Transformation of (per)chlorate into chloride by a newly isolated bacterium: reduction and dismutation. Appl. Microbiol. Biotechnol. 45, 420-426 (1996).
48. Coates, J. D. et al. Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas. Nature 411, 1039-1043 (2001).
49. Zhang, H. S., Bruns, M. A. & Logan, B. E. Chemolithoautotrophic perchlorate reduction by a novel hydrogen-oxidizing bacterium. Environ. Microbiol. 4, 570-576 (2002).
50. Herman, D. C. & Frankenberger W. T. Jr. Bacterial reduction of perchlorate and nitrate in water. J. Environ. Qual. 28, 1018-1024 (1999).
51. Okeke, B. C., Giblin, T. & Frankenberger, W. T. Reduction of perchlorate and nitrate by salt tolerant bacteria. Environ. Pollut. 118, 357-363 (2002).
52. Waller, A. S., Cox, E. E. & Edwards, E. A. Perchlorate-reducing microorganisms isolated from contaminated sites. Environ. Microbiol. 6, 517-527 (2004).
53. Coates, J. D., Cole, K. A., Chakraborty, R., O'Connor, S. M. & Achenbach, L. A. The diversity and ubiquity of bacteria utilizing humic substances as an electron donor for anaerobic respiration. Appl. Environ. Microbiol. 68, 2445-2452 (2002).
54. Chaudhuri, S. K., Lack, J. G. & Coates, J. D. Biogenic magnetite formation through anaerobic biooxidation of Fe(II). Appl. Environ. Microbiol. 67, 2844-2848 (2001).
55. Lack, J. G., Chaudhuri, S. K., Chakrabory, R., Achenbach, L. A. & Coates, J. D. Anaerobic biooxidation of Fe(II) by Dechlorosoma suillum. Microb. Ecol. 43, 424-431 (2002).
56. Lack, J. G. et al. Immobilization of radionuclides and heavy metals through anaerobic biooxidation of Fe(II). Appl. Environ. Microbiol. 68, 2704-2710 (2002).
57. Achenbach, L. A., Bruce, R. A., Michaelidou, U. & Coates, J. D. Dechloromonas agitata gen. nov., sp. nov. and Dechlorosoma suillum gen. nov., sp. nov., two novel environmentally dominant (per)chlorate-reducing bacteria and their phylogenetic position. Int. J. Syst. Evol. Microbiol. 51, 527-533 (2001).
58. Achenbach, L. A. & Coates, J. D. Disparity between bacterial phylogeny and physiology. ASM News 66, 714-716 (2000).
59. Cummings, D. E., Caccavo F. Jr, Spring, S. & Rosenzweig, R. F. Ferribacterium limneticum gen. nov., sp. nov., an Fe(III)-reducing microorganism isolated from mining-impacted freshwater lake sediments. Arch. Microbiol. 171, 183-188 (1999).
60. Tan, Z. & Reinhold-Hurek, B. Dechlorosoma suillum Achenbach et al. 2001 is a later subjective synonym of Azospira oryzae Reinhold-Hurek and Hurek 2000. Int. J. Syst. Evol. Microbiol. 53, 1139-1142 (2003).
61. Coates, J. D., Bruce, R. A., Patrick, J. A. & Achenbach, L. A. Hydrocarbon bioremediative potential of (per)chlorate-reducing bacteria. Bioremed. J. 3, 323-334 (1999).
62. Bender, K. S., Rice, M. R., Fugate, W. H., Coates, J. D. & Achenbach, L. A. Metabolic primers for the detection of (per)chlorate-reducing bacteria in the environment. Appl. Environ. Microbiol. (in the press).
63. Logan, B. E. et al. Kinetics of perchlorate- and chlorate-respiring bacteria. Appl. Environ. Microbiol 67, 2499-2506 (2001).
64. Coates, J. D. in Bergey's Manual of Systematic Bacteriology (eds Brenner, D., Krieg, N., Staley, J. & Garrity, G.) (Springer-Verlag, New York, in the press).
65. Bender, K. S., O'Connor, S. M., Chakraborty, R., Coates, J. D. & Achenbach, L. A. The chlorite dismutase gene of Dechloromonas agitata strain CKB: sequencing, transcriptional analysis and its use as a metabolic probe. Appl. Environ. Microbiol. 68, 4820-4826 (2002).
66. Chaudhuri, S. K., O'Connor, S. M., Gustavson, R. L., Achenbach, L. A. & Coates, J. D. Environmental factors that control microbial perchlorate reduction. Appl. Environ. Microbiol. 68, 4425-4430 (2002).
67. Pollock, J., Achenbach, L. A. & Coates, J. D. Potential for in-situ bioremediation of perchlorate contaminated environments. Appl. Environ. Microbiol. (in the press).
68. Logan, B. E., Wu, J. & Unz, R. F. Biological perchlorate reduction in high-salinity solution. Wat. Res. 35, 3034-3038 (2001).
69. Bruce, R. A. MSc. Thesis (Department of Microbiology, Southern Illinois University, Carbondale, 1999).
70. Kengen, S. W. M., Rikken, G. B., Hagen, W. R., Van Ginkel, C. G. & Stams, A. J. M. Purification and characterization of (per chlorate reductase from the chlorate-respiring strain GR-1. J. Bacteriol. 181, 6706-6711 (1999).
71. van Ginkel, C., Rikken, G., Kroon, A. & Kengen, S. Purification and characterization of chlorite dismutase: a novel oxygen-generating enzyme. Arch. Microbiol. 166, 321-326 (1996).
72. Stenklo, K., Thorell, H. D., Bergius, H., Aasa, R. & Nilsson, T. Chlorite dismutase from Ideonella dechloratans. J. Biol. Inorgan. Chem. 6, 601-607 (2001).
73. O'Connor, S. M. & Coates, J. D. A universal immuno-probe for (per)chlorate-reducing bacteria. Appl. Environ. Microbiol. 68, 3108-3113 (2002).
74. Thorell, H. D., Karlsson, J., Portelius, E. & Nilsson, T. Cloning, characterisation, and expression of a novel gene encoding chlorite dismutase from Ideonella dechloratans. Biochim. Biophys. Acta 1577, 445-451 (2002).
75. Xu, J. L., Trimble, J. J. Steinberg, L. & Logan, B. E. Chlorate and nitrate reduction pathways are separately induced in the perchlorate-respiring bacterium Dechlorosoma sp. KJ and the chlorate-respiring bacterium Pseudomonas sp. PDA. Water Res. 38, 673-680 (2004).
76. Bender, K. S., Chakraborty, R., Belchik, S. M., Coates, J. D. & Achenbach, L. A. Sequencing and transcriptional analysis of a perchlorate reductase gene from Dechloromonas agitata. Appl. Environ. Microbiol. (in the press).
77. Wolterink, A. F. W. M., Jonker, A. B., Kengen, S. W. M. & Stams, A. J. M. Pseudomonas chloritidismutans, sp. nov., a non-denitrifying, chlorate-reducing bacterium. Int. J. Syst. Evol. Microbiol. 52, 2183-2190 (2002).
78. Danielsson-Thorell, H., Stenklo, K., Karlsson, J. & Nilsson, T. A gene cluster for chlorate metabolism in Ideonella dechloratans. Appl. Environ. Microbiol. 69, 5585-5592 (2003).
79. Wolterink, A. F. W. M. et al. Characterization of the chlorate reductase from Pseudomonas chloritidismutans. J. Bacteriol. 185, 3210-3213 (2003).
80. Coleman, M. L., Ader, M., Chaudhuri, S. & Coates, J. D. Microbial isotopic fractionation of perchlorate chlorine. Appl. Environ. Microbiol. 69, 4997-5000 (2003).
81. Woese, C. R. in The Prokaryotes (eds Balows, A., Truper, H. G., Dworkin, M., Harder, W. & Schleifer, K.-H.) 3-18 (Springer-Verlag, New York, 1992).
82. Coates, J. D. & Achenbach, L. A. in Manual of Environmental Microbiology (eds Hurst, C. J., Knudsen, G. R., McInerney, M. J., Stetzenbaach, L. D. & Walter, M. W.) 719-727 (ASM Press, Washington DC, 2001).
83. Bailey, N. J. L., Krouse, H. R., Evans, C. R. & Rogers, M. A. Alteration of crude oil by waters and bacteria - evidence from geochemical and isotope studies. Am. Assoc. Petrol. Geol. Bull. 57, 1276 (1973).
84. Ku, T. C. W., Walter, L. M., Coleman, M. L., Blake, R. E. & Martini, A. M. Coupling between sulfur recycling and syndepositional carbonate dissolution: evidence from oxygen and sulfur isotope composition of pore water sulfate, South Florida Platform, USA. Geochim. Cosmochim. Acta 63, 2529-2546 (1999).
85. Nissenbaum, A., Presley, B. J. & Kaplan, I. R. Early diagenesis in a reducing fjord, Saanich Inlet, British Columbia, I, Chemical and isotopic changes in major components of interstitial water. Geochim. Cosmochim. Acta 36, 1007-1027 (1972).
86. Jendrzejewski, N., Eggenkamp, H. G. M. & Coleman, M. L. Characterisation of chlorinated hydrocarbons from chlorine and carbon isotopic compositions: scope of application to environmental problems. Appl. Geochem. 16, 1021-1031 (2001).
87. Ahad, J. M. E., Lollar, B. S., Edwards, E. A., Slater, G. F. & Sleep, B. E. Carbon isotope fractionation during anaerobic biodegradation of toluene: implications for intrinsic bioremediation. Environ. Sci. Technol. 34, 892-896 (2000).
88. Cloud, P. E., Friedman, I. & Sesler, F. D. Microbiological fractionation of the hydrogen isotopes. Science 127, 1394 (1958).
89. Hall, J. A., Kalin, R. M., Larkin, M. J., Allen, C. C. R. & Harper, D. B. Variation in stable carbon isotope fractionation during aerobic degradation of phenol and benzoate by contaminant degrading bacteria. Org. Geochem. 30, 801-811 (1999).
90. Harrison, A. G. & Thode, H. G. Mechanism of the bacterial fractionation of sulphate from isotope fractionation studies. Faraday Soc. Trans. 54, 84 (1957).
91. 2 formation in a marine peudomonad. J. Mar. Biol 236, 2520 (1961).
92. Morasch, B., Richnow, H., Schink, B. & Meckenstock, R. Stable hydrogen and carbon isotope fractionation during microbial toluene degradation: mechanistic and environmental aspects. Appl. Environ. Microbiol. 67, 4842-4849 (2001).
93. Sturchio, N. C., Hatzinger, P. B., Arkins, M., Suh, C. & Heraty, L. Chlorine isotope fractionation during microbial reduction of perchlorate. Environ. Sci. Technol. 37, 3859-3863 (2003).
94. Reinhold-Hurek, B. & Hurek, T. Reassessment of the taxonomic structure of the diazotrophic genus Azoarcus sensu lato and description of three new genera and new species, Azovibrio restrictus gen. nov., sp. nov., Azospira oryzae gen. nov., sp. nov. and Azonexus fungiphilus gen. nov., sp. nov. Int. J. Syst. Evol. Microbiol. 50, 649-659 (2000).
95. Engelhard, M., Hurek, T. & Reinhold-Hurek, B. Preferential occurrence of diazotrophic endophytes, Azoarcus spp., in wild rice species and land races of Oryza sativa in comparison with modern races. Environ. Microbiol. 2, 131-141 (2000).