Biochemical and genomic facets on the dissimilatory reduction of radionuclides by microorganisms - A review

Minerals Engineering

Volumn 23, Issue 8, 2010, Pages 591-599

  Mohapatra, Bidyut R ^a   Dinardo, Orlando ^a   Gould, W Douglas ^a   Koren, David W ^a  

^a Natural Resources Canada   (Canada)

Author keywords

Bioreduction; Bioremediation; Microorganisms; Radionuclides; Radionuclides reduction pathways

Indexed keywords

ANAEROBIC MICROORGANISMS; AQUATIC LIFE; BEST MANAGEMENT PRACTICES; BIOREDUCTION; BIOREDUCTIONS; ECOLOGICAL NICHE; ENVIRONMENTALLY BENIGN; ENVIRONMENTALLY-FRIENDLY; ENZYMATIC SYSTEM; GENETIC PATHWAYS; GEOLOGICAL ENVIRONMENT; IN-SITU; OXIDOREDUCTASES; PHYLOGENETIC DIVERSITY; POTENTIAL APPLICATIONS; SUBSURFACE ENVIRONMENT; SUSTAINABLE TECHNOLOGY; TERATOGENIC EFFECT; TOXIC COMPOUNDS;

BIODEGRADATION; BIOREMEDIATION; BIOTECHNOLOGY; DETOXIFICATION; EFFLUENTS; GENES; MICROORGANISMS; NUCLEAR INDUSTRY; PLUTONIUM; POLLUTION; REDOX REACTIONS; WASTE MANAGEMENT;

RADIOISOTOPES;

EID: 77953127709     PISSN: 08926875     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mineng.2010.03.004     Document Type: Review

References (94)

1. Abdelouas A., Lutze W., and Nuttall H.E. Uranium contamination in the subsurface, characterization and remediation. Reviews in Mineralogy and Geochemistry 38 (1999) 433-473
2. Ahier B.A., and Tracy B.L. Radionuclides in the Great Lakes basin. Environmental Health Perspectives 103 (1995) 89-101
3. Anderson R.T., Vrionis H.A., Ortiz-Bernad I., Resch C.T., Long P.E., Dayvault R., Karp K., Marutzky S., Metzler D.R., Peacock A., White D.C., Lowe M., and Lovley D.R. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Applied and Environmental Microbiology 69 (2003) 5884-5891
4. Beliaev A.S., and Saffarini D.A. Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe (III) and Mn (IV) reduction. Journal of Bacteriology 180 (1998) 6292-6297
5. Bencheikh-Latmani R., Williams S.M., Haucke L., Criddle C.S., Wu L., Zhou J., and Tebo B.M. Global transcriptional profiling of Shewanella oneidensis MR-1 during Cr (VI) and U (VI) reduction. Applied and Environmental Microbiology 71 (2005) 7453-7460
6. Boukhalfa H., Icopini G.A., Reilly S.D., and Neu M.P. Plutonium (IV) reduction by the metal-reducing bacteria Geobacter metallireducens GS15 and Shewanealla oneidensis MR1. Applied and Environmental Microbiology 73 (2007) 5897-5903
7. Cataldo D.A., Garland T.R., Wildung R.E., and Fellows R.J. Comparative metabolic behaviour and interrelationships of Tc and S in soybean plants. Health Physics 57 (1989) 281-287
8. 13C-labeled acetate at the field scale: detection of microbes responsible for reduction of U (VI). Environmental Science and Technology 39 (2005) 9039-9048
9. Choppin G.R., Bond A.H., and Hromadka P.M. Redox speciation of plutonium. Journal of Radioanalytical and Nuclear Chemistry 219 (1997) 203-210
10. Clay R. Cold war-hot nukes-legacy of an era. Environmental Health Perspectives 109 (2001) A162-A169
11. Coates J.D., Councell T., Ellis D.J., and Lovley D.R. Carbohydrate oxidation coupled to Fe (III) reduction, a novel form of anaerobic metabolisms. Anaerobe 4 (1998) 277-282
12. Coates J.D., Bhupathiraju V.K., Achenbach L.A., McInerney M.J., and Lovley D.R. Geobacter hydrogenophilus and Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe (III)-reducers. International Journal of Systematic and Evolutionary Microbiology 51 (2001) 581-588
13. De Luca G., Philip P., Dermoun Z., Rousset M., and Vermeglio A. Reduction of technetium (VII) by Desulfovibrio fructosovorans is mediated by the nickel-iron hydrogenase. Applied and Environmental Microbiology 67 (2001) 4583-4587
14. Dorsch, W.R., Howe, R.F., Racaniello, V.J., Burke, J.E., Paquette, D.E., 2007. Groundwater remediation program at Brookhaven National Laboratory, Upton, New York. In: Fourteenth Conference on the Geology of Long Island and Metropolitan New York, SUNY at Stony Brooke, April 14, 2007.
15. Ewing, R.C., 1999. Radioactivity and the 20th century. In: Burns, P.C., Finch, R., (Eds.), Uranium: Mineralogy, Geochemistry and the Environment, vol. 38. Mineralogical Society of America, Washington, DC, pp. 1-21.
16. Finch, R.J. and Murakami, T., 1999. Systematic and paragenesis of uranium minerals. In: Burns, P.C., Finch, R., (Eds.), Uranium: Mineralogy, Geochemistry and the Environment, vol. 38, Mineralogical Society of America, Washington, DC, pp. 91-179.
17. Finneran K.T., Housewright M.E., and Lovley D.R. Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environmental Microbiology 4 (2002) 510-516
18. Francis A.J. Microbial mobilization and immobilization of plutonium. Journal of Alloys and Compounds 444-445 (2007) 500-505
19. Francis A.J., Dodge C.J., Lu F., Halada G.P., and Clayton C.R. XPS and XANES studies of uranium reduction by Clostridium sp. Environmental Science and Technology 28 (1994) 636-639
20. Francis A.J., Dodge C.J., and Gillow J.B. Reductive dissolution of Pu (IV) by Clostridium sp. Under anaerobic conditions. Environmental Science and Technology 42 (2008) 2355-2360
21. Gould, W.D. and Kapoor, A., 2003. The microbiology of acid mine drainage. In: Jambor, J.L., Blowes, D.W., Ritchie, A.I.M., (Eds.), Environmental Aspects of Mine Wastes. Mineral Association of Canada, British Columbia, Vancouver, pp. 203-226.
22. Groudev S.N., Bratcova S.G., and Komnitsas K. Treatment of waters polluted with radioactive elements and heavy metals by means of a laboratory passive system. Minerals Engineering 12 (1999) 261-270
23. Groudev S.N., Georgiev P.S., Spasova I.I., and Komnitsas K. Bioremediation of a soil contaminated with radioactive elements. Hydrometallurgy 59 (2001) 311-318
24. Heidelberg J.F., Paulsen I.T., Nelson K.E., Gaidos E.J., Nelson W.C., Read T.D., Eisen J.A., Seshadri R., Ward N., Methe B., et al. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nature Biotechnology 20 (2002) 1118-1123
25. Icopini G.A., Boukhalfa H., and Neu M.P. Biological reduction of Np (V) and Np (V) citrate by metal-reducing bacteria. Environmental Science Technology 41 (2007) 2764-2769
26. Icopini G.A., Lack J.G., Hersman L.E., Neu M.P., and Boukhalfa H. Plutonium (V/VI) reduction by the metal-reducing bacteria Geobacter metallireducens GS-15 and Shewanella oneidensis MR-1. Applied and Environmental Microbiology 75 (2009) 3641-3647
27. Istok J.D., Senko J.M., Krumholz L.R., Watson D., Bogle M.A., Peacock A., Chang Y.-J., and White D.C. In Situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer. Environmental Science and Technology 38 (2004) 468-475
28. Khijniak T.V., Medvedeva-Lyalikova N.N., and Simonoff M. Reduction of pertechnetate by haloalkaliphilic strains of Halomonas. FEMS Microbiology Ecology 44 (2003) 109-115
29. Khijniak T.V., Slobodkin A.I., Coker V., Renshaw J.C., Livens F.R., Bonch-Osmolovskaya E.A., Birkeland N.K., Medvedeva-Lyalikova N.N., and Lloyd J.R. Reduction of uranium (VI) phosphate during growth of the thermophilic bacterium Thermoterrabacterium ferrireducens. Applied and Environmental Microbiology 71 (2005) 6423-6426
30. Kieft T.L., Fredrickson J.K., Onstott T.C., Gorby Y.A., Kostandarithes H.M., Bailey T.J., Kennedy D.W., Li S.W., Plymale A.E., Spadoni C.M., and Gray M.S. Dissimilatory reduction of Fe (III) and other electron acceptors by a Thermus isolate. Applied and Environmental Microbiology 65 (1999) 1214-1421
31. Kim B.C., Leang C., Ding Y.H., Glaven R.H., Coppi M.V., and Lovley D.R. OmcF, a putative c-type monoheme outer membrane cytochrome required for the expression of other outer membrane cytochromes in Geobacter sulfurreducens. Journal of Bacteriology 187 (2005) 4505-4513
32. Kotegov K.V., Pavlov O.N., and Shvendov V.P. Technetium. Advances in Inorganic Chemistry and Radiochemistry (1968), Academic Press, New York pp. 1-90
33. Krieger K. NORM contamination - now you see it now you don't. Health Physics 89 (2005) S20-S21
34. Leang C., and Lovley D.R. Regulation of two highly similar genes, omcB and omcC, in a 10 kb chromosomal duplication in Geobacter sulfurreducens. Microbiology 151 (2005) 1761-1767
35. Leang C., Coppi M.V., and Lovley D.R. OmcB, a c-type polyheme cytochrome, involved in Fe (III) reduction in Geobacter sulfurreducens. Journal of Bacteriology 185 (2003) 2096-2103
36. Li X., and Krumholz L.R. Thioredoxin is involved in U (VI) and Cr (VI) reduction in Desulfovibrio desulfuricans G20. Journal of Bacteriology 191 (2009) 4924-4933
37. Lieser K.H. Radionuclides in the geosphere: sources, mobility, reactions in natural waters and interactions with solids. Radiochimica Acta 70/71 (1995) 355-375
38. Linking Legacies, Connecting the Cold War Nuclear Weapons Production Processes to Their Environmental Consequences. US Department of Energy, DOE/EM-0319, January 1997.
39. Lloyd J.R. Microbial reduction of metals and radionuclides. FEMS Microbiology Reviews 27 (2003) 411-425
40. Lloyd J.R., Cole J.A., and Macaskie L.E. Reduction and removal of heptavalent technetium from solution by Escherichia coli. Journal of Bacteriology 179 (1997) 2014-2021
41. Lloyd J.R., Ridley J., Khizniak T., Lyalikova N.N., and Macaskie L.E. Reduction of technetium by Desulfovibrio desulfuricans: biocatalyst characterization and use in a flowthrough bioreactor. Applied and Environmental Microbiology 65 (1999) 2691-2696
42. Lloyd J.R., Thomas G.H., Finlay J.A., Cole J.A., and Macaskie L.E. Microbial reduction of technetium by Escherichia coli and Desulfovibrio desulfuricans: enhancement via the use of high-activity strains and effect of process parameters. Biotechnology and Bioengineering 66 (1999) 122-130
43. Lloyd J.R., Sole V.A., Van Praagh C.V.G., and Lovley D.R. Direct and Fe (II)-mediated reduction of technetium by Fe (III)-reducing bacteria. Applied and Environmental Microbiology 66 (2000) 3743-3749
44. Lloyd J.R., Young P., and Macaskie L.E. Biological reduction and removal of Np (V) by two microorganisms. Environmental Science and Technology 34 (2000) 1297-1301
45. Lloyd J.R., Mabbett A.N., Williams D.R., and Macaskie L.E. Metal reduction by sulphate-reducing bacteria: physiological diversity and metal specificity. Hydrometallurgy 59 (2001) 327-337
46. Lloyd J.R., Chesnes J., Glasauer S., Bunker D.J., Livens F.R., and Lovley D.R. Reduction of actinides and fission products by Fe (III)-reducing bacteria. Geomicrobiology Journal 19 (2002) 103-120
47. Lloyd J.R., Leang C., Hodges-Myerson A.L., Coppi M.V., Cuifo S., Methe B., Sandler S.J., and Lovley D.R. Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochemical Journal 369 (2003) 153-161
48. Lloyd J.R., Renshaw J.C., May I., Livens F.R., Burke I.T., Mortimerc R.J.G., and Morris K. Biotransformation of radioactive waste: microbial reduction of actinides and fission products. Journal of Nuclear and Radiochemical Sciences 6 (2005) 17-20
49. Lovley D.R., and Coates J.D. Novel forms of anaerobic respiration of environmental relevance. Current Opinion in Microbiology 3 (2000) 252-256
50. Lovley D.R., Phillips E.J.P., Gorby Y.A., and Landa E. Microbial reduction of uranium. Nature 350 (1991) 413-416
51. Lovley D.R., Roden E.E., Philips E.J.P., and Woodward J.C. Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Marine Geology 113 (1993) 41-53
52. 3 of Desulfovibrio vulgaris. Applied and Environmental Microbiology 59 (1993) 3572-3576
53. Lovley D.R. Cleaning up with genomics: applying molecular microbiology to bioremediation. Nature Reviews Microbiology 1 (2003) 35-44
54. Lovley D.R., and Phillips E.J.P. Reduction of uranium by Desulfovibrio desulfuricans. Applied and Environmental Microbiology 58 (1992) 850-856
55. Luo J., Cirpka O.A., Wu W., Fienen M.N., Jardine P.M., Mehlhorn T.L., Watson D.B., Criddle C.S., and Kitanidis P.K. Mass-transfer limitations for nitrate removal in a uranium-contaminated aquifer. Environmental Science and Technology 39 (2005) 8453-8459
56. Lyalikova N.N., and Khizhnyak T.V. Reduction of heptavalent technetium by acidophilic bacteria of the genus Thiobacillus. Microbiologia 65 (1996) 468-473
57. Macaskie L.E. The application of biotechnology to the treatment of wastes produced from the nuclear fuel cycle: biodegradation and bioaccumulation as a means of treating radionuclide-containing streams. CRC Critical Reviews in Biotechnology 11 (1991) 41-112
58. Macaskie L.E., and Basnakova G. Microbially-enhanced chemisorption of heavy metals: a method for the bioremediation of solutions containing long-lived isotopes of neptunium and plutonium. Environmental Science and Technology 32 (1998) 184-187
59. Macaskie L.E., Lloyd J.R., Thomas R.A.P., and Tolley M.R. The use of microorganisms for the remediation of solutions contaminated with actinide elements, other nuclides, and organic contaminants generated by nuclear fuel cycle activities. Nuclear Energy 35 (1996) 257-271
60. Marshall M.J., Plymale A.E., Kennedy D.W., Shi L., Wang Z., Reed S.B., Dohnalkova A.C., Simonson C.J., Liu C., Saffarini D.A., Romine M.F., Zachara J.M., Beliaev A.S., and Fredrickson J.K. Hydrogenase- and outer membrane c-type cytochrome-facilitated reduction of technetium (VII) by Shewanella oneidensis MR-1. Environmental Microbiology 10 (2008) 125-136
61. Mehta T., Coppi M.V., and Lovley D.R. Outer membrane c-type cytochromes required for Fe (III) and Mn (IV) oxide reduction in Geobacter sulfurreducens. Applied and Environmental Microbiology 71 (2005) 8634-8641
62. Methé T., Nelson K.E., Eisen J.A., Paulsen I.T., Nelson W., Heidelberg J.F., Wu D., Wu M., Ward N., Beanan M.J., et al. Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302 (2003) 1967-1969
63. Mossman K.L. Restructuring nuclear regulations. Environmental Health Perspectives 111 (2003) 13-17
64. Moyes L.N., Jones M.J., Reed W.A., Livens F.R., Charnock J.M., Mosselmans J.F.W., Hennig C., Vaughan D.J., and Pattrick R.A.D. An X-ray absorption spectroscopy study of neptunium (V) reactions with mackinawite (FeS). Environmental Science and Technology 36 (2002) 179-183
65. Myers C.R., and Myers J.M. Cloning and sequence of cymA, a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1. Journal of Bacteriology 179 (1997) 1143-1152
66. Myers J.M., and Myers C.R. Isolation and sequence of omcA, a gene encoding a decaheme outer membrane cytochrome c of Shewanella putrefaciens MR-1, and detection of omcA homologous in other strains of S. putrefaciens. Biochimica et Biophysica Acta 1373 (1998) 237-251
67. NABIR. Natural and Accelerated Bioremediation Research program (NABIR). Bioremediation of metals and radionuclides ... what it is and how it works. In: Hazen T.C., Benson S.M., Metting F.B., Faison B., Palmisano A.C., and McCullough J. (Eds). NABIR Primer. second ed. (2003), Lawrence Berkeley National Laboratory, Berkeley, CA
68. Najem G.R., and Voyce L.K. Health-effects of a thorium waste disposal site. American Journal of Public Health 80 (1990) 478-480
69. Neu M.P., Icopini G.A., and Boukhalfa H. Plutonium speciation affected by environmental bacteria. Radiochimica Acta 93 (2005) 705-714
70. 3 mutant. Applied and Environmental Microbiology 68 (2002) 3129-3132
71. 3 of Desulfovibrio desulfuricans strain G20. Archives of Microbiology 181 (2004) 398-406
72. Peretrukhin, V.F., Kryutchkov, S.V., Silin, V.I., Silin, I.G., Tananaev, I.G., 1996. Technical basis for classification of low-activity waste fraction from Hanford site tanks, Rev. 2, Westinghouse Hanford Company, WHC-SD-WM-TI699.
73. Renshaw J.C., Lloyd J.R., and Livens F.R. Microbial interactions with actinides and long-lived fission products. Comptes Rendus Chimie 10 (2007) 1067-1077
74. Rittmann B.E., Banaszak J.E., and Reed D.T. Reduction of Np (V) and precipitation of Np (IV) by an anaerobic microbial consortium. Biodegradation 13 (2002) 329-342
75. Rossmann R., Sawers G., and Böck A. Mechanism of regulation of the formate-hydrogenlyase pathway by oxygen, nitrate, and pH: definition of the formate regulon. Molecular Microbiology 5 (1991) 2807-2814
76. Russin P.A., Quintana L., Brainard J.R., Strietelmeier B.A., Tait C.D., Ekberg S.A., Palmer P.D., Newton T.W., and Clark D.L. Solubilization of plutonium hydrous oxide by iron-reducing bacteria. Environmental Science and Technology 28 (1994) 1686-1690
77. Sani R.K., Peyton B.M., Smith W.A., Apel W.A., and Petersen J.N. Dissimilatory reduction of Cr (VI), Fe (III), and U (VI) by Cellulomonas isolates. Applied Microbiology and Biotechnology 60 (2002) 192-199
78. Sauter M., Bohm R., and Böck A. Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Molecular Microbiology 6 (1992) 1523-1532
79. Sawers G. The hydrogenases and formate dehydrogenases of Escherichia coli. Antonie van Leeuwenhoek 66 (1994) 57-88
80. Shelobolina E.S., Sullivan S.A., O'Neill K.R., Nevin K.P., and Lovley D.R. Isolation, characterization, and U(VI)-reducing potential of a facultatively anaerobic, acid-resistant bacterium from low-pH, nitrate- and U(VI)-contaminated subsurface sediment and description of Salmonella subterranea sp. nov. Applied and Environmental Microbiology 70 (2004) 2959-2965
81. Shelobolina E.S., Coppi M.V., Korenevsky A.A., DiDonato L.N., Sullivan S.A., Konishi H., Xu H., Leang C., Butler J.E., Kim B.-C., and Lovley D.R. Importance of c-type cytochromes for U (VI) reduction by Geobacter sulfurreducens. BMC Microbiology 7 (2007) 1-15
82. Shyu J.B.H., Lies D.P., and Newman D.K. Protective role of tolC in efflux of the electron shuttle anthraquinone-2,6-disulfonate. Journal of Bacteriology 184 (2002) 1806-1810
83. Simonoff M., Sergeant C., Poulain S., and Pravikoff M.S. Microorganisms and migration of radionuclides in environment. Comptes Rendus Chimie 10 (2007) 1092-1097
84. Suzuki Y., Kelly S.D., Kemner K.M., and Banfield J.F. Microbial populations stimulated from hexavalent uranium reduction in uranium mine sediment. Applied and Environmental Microbiology 69 (2003) 1337-1346
85. Suzuki Y., Kelly S.D., Kemner K.M., and Banfield J.F. Direct microbial reduction and subsequent preservation of uranium in natural near-surface sediment. Applied and Environmental Microbiology 71 (2005) 1790-1797
86. Tabak H.H., Lens P., van Hullebusch E.D., and Dejonghe W. Developments in bioremediation of soils and sediments polluted with metals and radionuclides - 1. Microbial processes and mechanisms affecting bioremediation of metal contamination and influencing metal toxicity and transport. Reviews in Environmental Science and Biotechnology 4 (2005) 115-156
87. Tamura K., Dudley J., Nei M., and Kumar S. MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24 (2007) 1596-1599
88. Tebo B.M., and Obraztsova A.Y. Sulfate-reducing bacterium grows with Cr (VI), U (VI), Mn (IV), and Fe (III) as electron acceptors. FEMS Microbiology Letters 162 (1998) 193-198
89. US DOE, 2005. Genomics: GTL Roadmap, Office of Science. US Department of Energy, August 2005, Appendix B.
90. US EPA, 2000. Radionuclides in Drinking Water Rule. US Environmental Protection Agency. (accessed 15.09.09).
91. Wade R., and DiChristina T.J. Isolation of U (VI) reduction-deficient mutants of Shewanella putrefaciens. FEMS Microbiology Letters 184 (2000) 143-148
92. Watts R.J. Hazardous Wastes: Sources, Pathways, Receptors (1998), John Wiley & Sons, New York
93. Whicker F.W., Hinton T.G., MacDonell M.M., Pinder J.E., and Habegger L.J. Avoiding destructive remediation at DOE sites. Science 303 (2004) 1615-1616
94. Wildung R.E., Gorby Y.A., Krupka K.M., Hess N.J., Li S.W., Plymale A.E., McKinley J.P., and Fredrickson J.K. Effect of electron donor and solution chemistry on products of dissimilatory reduction of technetium by Shewanella putrefaciens. Applied and Environmental Microbiology 66 (2000) 2451-2460