Uranium reduction and resistance to reoxidation under iron-reducing and sulfate-reducing conditions

Water Research

Volumn 43, Issue 18, 2009, Pages 4652-4664

  Boonchayaanant, Benjaporn ^a   Nayak, Dipti ^a   Du, Xin ^a   Criddle, Craig S ^a  

^a Stanford University   (United States)

Author keywords

Clostridium; Desulfovibrio; Ferrous iron; Nitrate; Oxygen; Uranium reoxidation

Indexed keywords

BIOREMEDIATION; CLOSTRIDIUM; GROUNDWATER; IRON RESEARCH; NITRATES; OXYGEN; RNA; SULFUR COMPOUNDS; URANIUM COMPOUNDS;

16S RRNA GENE CLONE LIBRARIES; DESULFOVIBRIO; FERROUS IRON; FIELD RESEARCH CENTERS; RE-OXIDATION; SULFATE REDUCING; SULFATE-REDUCING CONDITIONS; URANIUM REDUCTION;

IRON COMPOUNDS;

GROUND WATER; IRON; NITRATE; OXYGEN; RNA 16S; SULFATE; URANIUM; WATER;

BIOREMEDIATION; ENRICHMENT; GROUNDWATER; IRON-REDUCING BACTERIUM; MOBILIZATION; NITRATE; OXIDATION; OXYGEN; RNA; SEDIMENT; SULFATE-REDUCING BACTERIUM; URANIUM;

ARTICLE; BIOREMEDIATION; CLOSTRIDIUM; CONTROLLED STUDY; DESULFOVIBRIO; ELECTRON; ENRICHMENT CULTURE; GENE LIBRARY; MOLECULAR STABILITY; OXIDATION; PRIORITY JOURNAL; REDUCTION; SEDIMENT; SULFATE REDUCING BACTERIUM; UNITED STATES;

CLOSTRIDIUM; DESULFOVIBRIO;

EID: 71749098364     PISSN: 00431354     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.watres.2009.07.013     Document Type: Article

References (55)

1. Abdelouas A., Lutze W., and Nuttall H.E. Oxidative dissolution of uraninite precipitated on Navajo sandstone. Journal of Contaminant Hydrology 36 (1999) 353-375
2. Akob D.M., Mills H.J., and Kostka J.E. Metabolically active microbial communities in uranium-contaminated subsurface sediments. FEMS Microbial Ecology 59 1 (2007) 95-107
3. Anderson R.T., and Lovley D.R. Microbial redox interactions with uranium: an environmental perspective. In: Keith-Roach M.J., and Livens F.R. (Eds). Interactions of Microorganisms with Radionuclides (2002), Elsevier, Oxford, UK 205-223
4. 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
5. Andreesen J.R., Bahl H., and Gottschalk G. Introduction to the Physiology and Biochemistry of the Genus Clostridium. In: Minton N.P., and Clark D.J. (Eds). Clostridia (1989), Plenum Press, New York 27-62
6. Beller H.R. Anaerobic, nitrate-dependent oxidation of U(IV) oxide minerals by the chemolithoautotrophic bacterium Thiobacillus denitrificans. Applied and Environmental Microbiology 71 4 (2005) 2170-2174
7. Boonchayaanant, B., Gu, B., Wang, W., Ortiz, M.E., Criddle, C.S., Microbially-generated hydrogen sulfide can account for the rates of U(VI) reduction by a sulfate-reducing bacterium. Biodegradation Journal, in press (published online July 14, 2009)
8. Bradford M.M. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Analytical Biochemistry 72 (1976) 248-454
9. Coates J.D., Phillips E.J., Lonergan D.J., Jenter H., and Lovley D.R. Isolation of Geobacter species from diverse sedimentary environments. Applied and Environmental Microbiology 62 5 (1996) 1531-1536
10. Dobbin P.S., Carter J.P., San Juan C.G., Hobe M.V., Powell A.K., and Richardson D.J. Dissimilatory Fe(III) reduction by Clostridium beijerinckii isolated from freshwater sediment using Fe(III) maltol enrichment. FEMS Microbiology Letters 176 (1999) 131-138
11. Finneran K.T., Housewright M.E., and Lovley D.R. Multiple influence of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environmenal Microbiology 4 9 (2002) 510-516
12. Francis A.J., and Dodge C.J. Anaerobic microbial dissolution of transition and heavy metal oxides. Applied and Environmental Microbiology 54 4 (1988) 1009-1014
13. Francis A.J., and Dodge C.J. Anaerobic microbial remobilization of toxic metals coprecipitated with iron oxide. Environmental Science & Technology 24 3 (1990) 373-378
14. 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. Environmenal Science & Technology 28 (1994) 636-639
15. Gao W., and Francis A.J. Reduction of uranium(VI) to uranium(VI) by Clostridia. Applied and Environmental Microbiology 74 14 (2008) 4580-4584
16. Gorby Y.A., and Lovley Y.A.G. Enzymatic uranium precipitation. Environmental Science & Technology 26 (1992) 206-207
17. Green D.W., and Perry R.H. Perry's Chemical Engineers' Handbook. eighth ed. (2007), McGraw-Hill, New York
18. Hasan S.M., and Hall J.B. Physiological function of nitrate reduction in Clostridium perfringens. The Journal of General Microbiology 87 1 (1975) 120-128
19. Holmes D.E., Finneran K.T., O'Neil R.A., and Lovley D.R. Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer sediments. Applied and Environmental Microbiology 68 5 (2002) 2300-2306
20. Hua B., Xu H., Terry J., and Deng B. Kinetics of uranium (VI) reduction by hydrogen sulfide in anoxic aqueous system. Environmental Science & Technology 40 (2006) 4666-4671
21. Hwang C., Wu W., Gentry T.J., Carley J., Corbin G.A., Carroll S.L., Watson D.B., Jardine P.M., Zhou J., Criddle C.S., and Fields M.W. Bacterial community succession during in situ uranium bioremediation: spatial similarities along controlled flow paths. The International Society for Microbial Ecology Journal 3 (2009) 47-64
22. Keith S.M., and Herbert R.A. Dissimilatory nitrate reduction by a strain of Desulfovibrio desulfuricans. FEMS Microbiology Letters 18 (1983) 55-59
23. Keith S.M., MacFarlane G.T., and Herbert R.A. Dissimilatory nitrate reduction by a strain of Clostridium butyricum Isolated from estuarine sediments. Archives of Microbiology 132 (1982) 62-66
24. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5 (2004) 150-163
25. Liger E., Charlet L., and Cappellen P.V. Surface catalysis of uranium(VI) reduction by iron(II). Geochimica et Cosmochimica Acta 63 (1999) 2939-2955
26. Lin B., Hyacinthe C., Bonneville S., Braster M., Cappellen P.V., and Roling W.F.M. Phylogenetic and physiological diversity of dissimilatory ferric iron reducers in sediments of the polluted Scheldt estuary, Northwest Europe. Environmental Microbiology 9 8 (2007) 1956-1968
27. Lovley D.R., and Phillips E.J.P. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Applied and Environmental Microbiology 54 6 (1988) 1472-1480
28. Lovley D.R., Phillips E.J.P., Gorby Y.A., and Landa E.R. Microbial reduction of uranium. Nature 350 (1991) 413-416
29. Lovley D.R., and Phillips E.J.P. Reduction of uranium by Desulfovibrio desulfuricans. Applied and Environmental Microbiology 58 (1992) 850-856
30. Lovley D.R., Roden E.E., Phillips E.J.P., and Woodward J.C. Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Marine Geology 113 (1993) 41-53
31. Lovley D.R., Giovannoni S.J., White D.C., Champine J.E., Phillips E.J.P., Gorby Y.A., and Goodwin S. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Archives of Microbiology 159 (1993) 336-344
32. Madden A.S., Smith A.C., Balkwill D.L., Fagan L.A., and Phelps T.J. Microbial uranium immobilization independent of nitrate reduction. Environmental Microbiology 9 9 (2007) 2321-2330
33. Murillo M., Gugliuzza F., Senko J., Basu P., and Stolz J.F. A heme-C-containing enzyme complex that exhibits nitrate and nitrite reductase activity from the dissimilatory iron-reducing bacterium Geobacter metallireducens. Archives of Microbiology 172 (1999) 313-320
34. McCormick M.L., and Adriaens P. Carbon tetrachloride transformation on the surface of nanoscale biogenic magnetite particles. Environmental Science & Technology 38 (2004) 1045-1053
35. McCullough J., Hazen T.C., Benson S.M., Metting F.B., and Palmisano A.C. Bioremediation of Metals and Radionuclides: What It Is and How It Works (1999), Lawrence Berkeley National Laboratory, California
36. Moon H.S., Komlos J., and Jaffe P.R. Uranium reoxidation in previously bioreduced sediment by dissolved oxygen and nitrate. Environmental Science & Technology 41 (2007) 4587-4592
37. Nyman J.L., Marsh T.L., Ginder-Vogel M.A., Gentile M., Fendorf S., and Criddle C.S. Heterogeneous response to biostimulation for U(VI) reduction in replicated sediment microcosms. Biodegradation 17 (2006) 303-316
38. Nyman J., Gentile M., and Criddle C. Sulfate requirement for the growth of U(VI)-reducing bacteria in an ethanol-fed enrichment. Bioremediation Journal 11 1 (2007) 21-32
39. Nyman J.L., Wu H., Gentile M.E., Kitanidis P.K., and Criddle C.S. Inhibition of a U(VI)- and sulfate-reducing consortia by U(VI). Environmental Science & Technology 41 18 (2007) 6528-6533
40. 2 nanoparticles. Environmental Science & Technology 37 (2003) 721-727
41. Park H.S., Kim B.H., Kim H.S., Kim H.J., Kim G.T., Chang I.S., Park Y.K., and Chang H.I. A novel electrochemically active and Fe(III)-reducing bacterium phylogenetically related to Clostridium butyricum isolated from a microbial fuel cell. Anaerobe 7 (2001) 297-306
42. Schink B. Clostridium magnum sp. nov., a non-autotrophic homoacetogenic bacterium. Archives of Microbiology 137 (1984) 250-255
43. Seitz H.-J., and Cypionka H. Chemolithotrophic growth of Desulfovibrio desulfuricans with hydrogen coupled to ammonification of nitrate or nitrite. Archives of Microbiology 146 (1986) 63-67
44. Senko J.M., Istok J.D., Suflita J.M., and Krumholz L.R. In-situ evidence for uranium immobilization and remobilization. Environmental Science & Technology 36 7 (2002) 1491-1496
45. Senko J.M., Mohamed Y., Dewers T.A., and Krumholz L.R. Role of Fe(III) minerals in nitrate-dependent microbial U(IV) oxidation. Environmental Science & Technology 39 (2005) 2529-2536
46. Senko J.M., Kelly S.D., Dohnalkova A.C., McDonough J.T., Kemner K.M., and Burgos W.D. The effect of U(IV) bioreduction kinetics on subsequent reoxidation of biogenic U(IV). Geochemica et Cosmochimica Acta 71 (2007) 4644-4654
47. Stookey L.L. Ferrozine - a new spectrophotometric reagent for iron. Analytical Chemistry 42 7 (1970) 779-781
48. Straub K.L., and Buchholz-Cleven B.E.E. Geobacter bremensis sp. nov. and Geobacter pelophilus sp. nov., two dissimilatory ferric-iron-reducing bacteria. International Journal of Systematic and Evolutionary Microbiology 51 (2001) 1805-1808
49. Sung Y., Fletcher K.E., Ritalahti K.M., Apkarian R.P., Ramos-Hernandez N., Sanford R.A., Mesbah N.M., and Loffler F.E. Geobacter lovleyi sp. nov. strain SZ, a novel metal-reducing and tetrachloroethene-dechlorinating bacterium. Applied and Environmental Microbiology 72 4 (2006) 2775-2782
50. 3 in energy production system. Archives of Microbiology 125 (1980) 35-42
51. Voordouw G. Carbon monoxide cycling by Desulfovibrio vulgaris Hildengorough. Journal of Bacteriology 184 21 (2002) 5903-5911
52. Widdel F., and Pfennig N. Dissimilatory sulfate-or sulfur-reducing bacteria. In: Krieg N.R., and Holt J.G. (Eds). Bergey's Manual of Systematic Bacteriology. ninth ed. vol. I (1984), Williams & Wilkins, Baltimore, London 663-679
53. Wu W.M., Carley J., Fienen M., Mehlhorn T., Lowe K., Nyman J., Luo J., Gentile M.E., Rajan J., Wagner D., Hickey R.F., Gu B., Watson D., Cirpka O.A., Kitanidis P.K., Jardine P., and Criddle C.S. Pilot-scale in situ bioremediation of uranium in a highly contaminated aquifer. 1. Conditioning of a treatment zone. Environmental Science & Technology 40 (2006) 3978-3985
54. Wu W.M., Carley J., Gentry T., Ginder-Vogel M.A., Fienen M., Mehlhorn T., Yan H., Caroll S., Pace M.N., Nyman J., Luo J., Gentile M.E., Fields M.W., Hickey R.F., Gu B., Watson D., Cirpka O.A., Zhou J., Fendorf S., Kitanidis P.K., Jardine P., and Criddle C.S. Pilot-scale in situ bioremediation of uranium in a highly contaminated aquifer. 2. Reduction of U(VI) and geochemical control of U(VI) bioavailability. Environmental Science & Technology 40 (2006) 3986-3995
55. Wu W.M., Carley J., Luo J., Ginder-Vogel M., Cardenas E., Leigh M.B., Hwang C., Kelly S.D., Ruan C., Wu L., van Nostand J., Gentry T., Lowe K., Melhourne T., Carroll S., Fields M.W., Gu B., Watson D., Kemner K.M., Marsh T.L., Tiedje J., Zhou J., Fendorf S., Kitanidis P.K., Jardine P.M., and Criddle C.S. In situ bioreduction of uranium (VI) to submicromolar levels and reoxidation by dissolved oxygen. Environmental Science & Technology 41 (2007) 5716-5723