Effects of microbial community structure, terminal electron accepting conditions, and molybdate on the extent of U(VI) reduction in landfill aquifer sediments

Geomicrobiology Journal

Volumn 28, Issue 5-6, 2011, Pages 430-443

  Spain, Anne M ^a   Peacock, Aaron D ^b   Krumholz, Lee R ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

^b HALEY AND ALDRICH INC   (United States)

Author keywords

Bioremediation; Molybdate; Nicrobial communities; Polar lipid fatty acid (plfa) analysis; Uranium reduction

Indexed keywords

AQUIFER; BIOREMEDIATION; COMMUNITY STRUCTURE; FATTY ACID; GEOCHEMISTRY; IMMOBILIZATION; LANDFILL; MICROBIAL COMMUNITY; MOLYBDATE GROUP; SEDIMENT POLLUTION; URANIUM;

EID: 79960792594     PISSN: 01490451     EISSN: 15210529     Source Type: Journal    
DOI: 10.1080/01490451.2010.507643     Document Type: Article

References (64)

1. Abdelouas A, Lutze W, Gong W, Nuttall EH, Strietelmeier BA, Travis BJ. 2000. Biological reduction of uranium in groundwater and subsurface soil. Sci Total Environ 250:21-35.
2. Akob DM, Mills HJ, Gihring TM, Kerkhof L, Stucki JW, Anastacio AS, Chin KJ, Kusel K, Palumbo AV, Watson DB, Kostka JE. 2008. Functional diversity and electron donor dependence of microbial populations capable of U(VI) reduction in radionuclide-contaminated subsurface sediments. Appl Environ Microbiol 74:3159-3170.
3. Anderson RT, Vrionis HA, Ortiz-Bernad I, Resch CT, Long PE, Dayvault R, Karp K, Marutzky S, Metzler DR, Peacock A, White DC, Lowe M, Lovley DR. 2003. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl Environ Microbiol 69:5884-5891.
4. Baldwin BR, Peacock AD, Park M, Ogles DM, Istok JD, McKinley JP, Resch CT,White DC. 2008. Multilevel samplers as microcosms to assess microbial response to biostimulation. Ground Water 46:295-304.
5. Balkwill DL, Leach FR, Wilson JT, McNabb JF, White DC. 1988. Equivalence of microbial biomass measures based on membrane lipid and cell wall components, adenosine triphosphate, and direct counts in subsurface aquifer sediments. Microb Ecol 16:73-84.
6. Basu SK, Oleszkiewicz JA, Sparling R. 2005. Effect of sulfidogenic and methanogenic inhibitors on reductive dehalogenation of 2-chlorophenol. Environ Technol 26:1383-1391.
7. Beeman RE, Suflita JM. 1987. Microbial ecology of a shallow unconfined ground water aquifer polluted by municipal landfill leachate. Microb Ecol 14:39-54.
8. Behrends T, Van Cappellen P. 2005. Competition between enzymatic and abiotic reduction of uranium(VI) under iron reducing conditions. Chem Geol 220:315-327.
9. Bligh EG, Dryer WJ. 1954. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911-917.
10. Boonchayaanant B, Gu B, Wang W, Ortiz ME, Criddle CS. 2009. Can microbially-generated hydrogen sulfide account for the rates of U(VI) reduction by a sulfate-reducing bacterium? Biodegradation 21:81-95.
11. Cappenberg TE. 1974. Interrelations between sulfate-reducing and methaneproducing bacteria in bottom deposits of a fresh-water lake. II. Inhibition experiments. Antonie Van Leeuwenhoek 40:297-306.
12. Cardenas E, WuWM, LeighMB, Carley J, Carroll S, Gentry T, Luo J, Watson D, Gu B, Ginder-VogelM, Kitanidis PK, Jardine PM, Zhou J, Criddle CS, Marsh TL, Tiedje JM. 2008. Microbial communities in contaminated sediments, associated with bioremediation of uranium to submicromolar levels. Appl Environ Microbiol 74:3718-3729.
13. Chang YJ, Long PE, Geyer R, Peacock AD, Resch CT, Sublette K, Pfiffner S, Smithgall A, Anderson RT, Vrionis HA, Stephen JR, Dayvault R, Ortiz-Bernad I, Lovley DR, White DC. 2005. Microbial incorporation of 13Clabeled acetate at the field scale: detection of microbes responsible for reduction of U(VI). Environ Sci Technol 39:9039-9048.
14. Cozzarelli IM, Suflita JM, Ulrich GA, Harris SH, Scholl MA, Schlottmann JL, Christenson S. 2000. Geochemical and microbiological methods for evaluating anaerobic processes in an aquifer contaminated by landfill leachate. Environ Sci Technol 34:4025-4033.
15. El Fantroussi S, Ntibahezwa E, Thomas S, Naveau H, Agathos SN. 1998. Effect of specific inhibitors on the anaerobic reductive dechlorination of 2,4,6- trichlorophenol by a stable methanogenic consortium. Anaerobe 4:197-203.
16. Elias DA, Krumholz LR,Wong D, Long PE, Suflita JM. 2003a. Characterization of microbial activities and U reduction in a shallow aquifer contaminated by uranium mill tailings. Microb Ecol 46:83-91.
17. Elias DA, Senko JM, Krumholz LR. 2003b. A procedure for quantitation of total oxidized uranium for bioremediation studies. J Microbiol Methods 53:343-353.
18. Francis AJ, Dodge CJ, Lu F, Halada GP, Clayton CR. 1994. XPS and XANES Studies of Uranium Reduction by Clostridium sp. Environ Sci Technol 28:636-639.
19. Fredrickson JK, Kostandarithes HM, Li SW, Plymale AE, Daly MJ. 2000a. Reduction of Fe(III), Cr(VI), U(VI), and Tc(VII) by Deinococcus radiodurans R1. Appl Environ Microbiol 66:2006-2011.
20. Fredrickson JK, Zachara JM, Kennedy DW, Duff MC, Gorby YA, Li SW, Krupka KM. 2000b. Reduction of U(VI) in goethite (α-FeOOH) suspensions by a dissimilatory metal-reducing bacterium. Geochim Cosmochim Acta 64:3085-3098.
21. Gao W, Francis AJ. 2008. Reduction of uranium(VI) to uranium(IV) by clostridia. Appl Environ Microbiol 74:4580-4584.
22. Gu B, Liang L, Dickey MJ, Yin X, Dai S. 1998. Reductive precipitation of uranium(VI) by zero-valent iron. Environ Sci Technol 32:3366-3373.
23. Gu B, Yan H, Zhou P, Watson DB, Park M, Istok J. 2005. Natural humics impact uranium bioreduction and oxidation. Environ Sci Technol 39:5268-5275.
24. Guckert JB, Antworth CP, Nichols PD, White DC. 1985. Phospholipid, esterlinked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediment. FEMS Microbiol Ecol 31:147-158.
25. Hedrick DB, Peacock AD, Lovley DR,Woodard TL, Nevin KP, Long PE,White DC. 2009. Polar lipid fatty acids, LPS-hydroxy fatty acids, and respiratory quinones of three Geobacter strains, and variation with electron acceptor. J Ind Microbiol Biotechnol 36:205-209.
26. Henson JM, McInerney MJ, Beaty PS, Nickels J, White DC. 1988. Phospholipid fatty acid composition of the syntrophic anaerobic bacterium Syntrophomonas wolfei. Appl Environ Microbiol 54:1570-1574.
27. Holmes DE, Finneran KT, O'Neil RA, Lovley DR. 2002. Enrichment of members of the family Geobacteraceae associated with stimulation of dissimilatory metal reduction in uranium-contaminated aquifer sediments. Appl Environ Microbiol 68:2300-2306.
28. Hua B, Deng B. 2008. Reductive immobilization of uranium(VI) by amorphous iron sulfide. Environ Sci Technol 42:8703-8708.
29. Hwang C, Wu W, Gentry TJ, Carley J, Corbin GA, Carroll SL, Watson DB, Jardine PM, Zhou J, Criddle CS, Fields MW. 2009. Bacterial community succession during in situ uranium bioremediation: spatial similarities along controlled flow paths. ISME J 3:47-64.
30. Istok JD, Senko JM, Krumholz LR, Watson D, Bogle MA, Peacock A, Chang YJ, White DC. 2004. In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer. Environ Sci Technol 38:468-475.
31. Khijniak TV, Slobodkin AI, Coker V, Renshaw JC, Livens FR, Bonch-Osmolovskaya EA, Birkeland NK, Medvedeva-Lyalikova NN, Lloyd JR. 2005. Reduction of uranium(VI) phosphate during growth of the thermophilic bacterium Thermoterrabacterium ferrireducens. Appl Environ Microbiol 71:6423-6426.
32. Liu C, Gorby YA, Zachara JM, Fredrickson JK, Brown CF. 2002. Reduction kinetics of Fe(III), Co(III), U(VI), Cr(VI), and Tc(VII) in cultures of dissimilatory metal-reducing bacteria. Biotechnol Bioeng 80:637-649.
33. Lovley DR, Phillips EJ. 1986. Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol 51:683-689.
34. Lovley DR, Phillips EJ. 1987. Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536-1540.
35. Lovley DR, Phillips EJ. 1992a. Reduction of uranium by Desulfovibrio desulfuricans. Appl Environ Microbiol 58:850-856.
36. Lovley DR, Phillips EJP. 1992b. Bioremediation of uranium contaminationwith enzymatic uranium reduction. Environ Sci Technol 26:2228-2234.
37. Lovley DR, Phillips EJP, Gorby YA, Landa ER. 1991. Microbial reduction of uranium. Nature 350.
38. Lovley DR, Roden EE, Phillips EJP, Woodward JC. 1993. Enzymic iron and uranium reduction by sulfate-reducing bacteria. Mar Geology 113:41-53.
39. Luo W, Wu WM, Yan T, Criddle CS, Jardine PM, Zhou J, Gu B. 2007. Influence of bicarbonate, sulfate, and electron donors on biological reduction of uranium and microbial community composition. Appl Microbiol Biotechnol 77:713-721.
40. Madden AS, Palumbo AV, Ravel B, Vishnivetskaya TA, Phelps TJ, Schadt CW, Brandt CC. 2009. Donor-dependent extent of uranium reduction for bioremediation of contaminated sediment microcosms. J EnvironQual 38:53-60.
41. Mohanty SR, Kollah B, Hedrick DB, Peacock AD, Kukkadapu RK, Roden EE. 2008. Biogeochemical processes in ethanol stimulated uranium-contaminated subsurface sediments. Environ Sci Technol 42:4384-4390.
42. Nevin KP, Finneran KT, Lovley DR. 2003. Microorganisms associated with uranium bioremediation in a high-salinity subsurface sediment. Appl Environ Microbiol 69:3672-3675.
43. North NN, Dollhopf SL, Petrie L, Istok JD, Balkwill DL, Kostka JE. 2004. Change in bacterial community structure during in situ biostimulation of subsurface sediment cocontaminated with uranium and nitrate. Appl Environ Microbiol 70:4911-4920.
44. Nyman JL, Marsh TL, Ginder-Vogel MA, Gentile M, Fendorf S, Criddle C. 2006. Heterogeneous response to biostimulation for U(VI) reduction in replicated sediment microcosms. Biodegradation 17:303-316.
45. Oremland RS, Capone DG. 1988. Use of specific inhibitors in biogeochemistry and microbial ecology. Adv Microb Ecol 10:285-383.
46. Peacock AD, Chang YJ, Istok JD, Krumholz L, Geyer R, Kinsall B, Watson D, Sublette KL, White DC. 2004. Utilization of microbial biofilms as monitors of bioremediation. Microb Ecol 47:284-292.
47. Petrie L, North NN, Dollhopf SL, Balkwill DL, Kostka JE. 2003. Enumeration and characterization of iron(III)-reducing microbial communities from acidic subsurface sediments contaminated with uranium(VI). Appl Environ Microbiol 69:7467-7479.
48. Pinkart HC, Ringelberg DB, Piceno YM, MacNaughton SJ, White DC. 2002. Biochemical approaches to biomass measurements and community structure analysis. In: Hurst CJ, Crawford RL, Knudsen GR, McInerney MJ, Stetzenbach LD, editors. Manual of Environmental Microbiology Second Edition. Washington, DC: ASM Press. P 101-113.
49. Senko JM, Istok JD, Suflita JM, Krumholz LR. 2002. In-situ evidence for uranium immobilization and remobilization. Environ Sci Technol 36:1491-1496.
50. Senko JM, Zhang G, McDonough JT, Bruns MA, Burgos WD. 2009. Metal reduction at low pH by a Desulfosporosinus species: Implications for the biological treatment of acid mine drainage. Geomicrobiol J 26:71-82.
51. Shelobolina ES, Sullivan SA, O'Neill KR, Nevin KP, Lovley DR. 2004. 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. Appl Environ Microbiol 70:2959-2965.
52. Shelobolina ES, Vrionis HA, Findlay RH, Lovley DR. 2008. Geobacter uraniireducens sp. nov., isolated from subsurface sediment undergoing uranium bioremediation. Int J Syst Evol Microbiol 58:1075-1078.
53. Spain AM, Peacock AD, Istok JD, Elshahed MS, Najar FZ, Roe BA, White DC, Krumholz LR. 2007. Identification and isolation of a Castellaniella species important during biostimulation of an acidic nitrate- and uraniumcontaminated aquifer. Appl Environ Microbiol 73:4892-4904.
54. Sung Y, Fletcher KE Ritalahti KM, Apkarian RP, Ramos-Hernandez N, Sanford RA, Mesbah NM, Loffler FE. 2006. Geobacter lovleyi sp. nov. strain SZ, a novel metal-reducing and tetrachloroethene-dechlorinating bacterium. Appl Environ Microbiol 72:2775-2782.
55. Suzuki Y, Kelly SD, Kemner KM, Banfield JF. 2003. Microbial populations stimulated for hexavalent uranium reduction in uranium mine sediment. Appl Environ Microbiol 69:1337-1346.
56. Suzuki Y, Kelly SD, Kemner KM, Banfield JF. 2005. Direct microbial reduction and subsequent preservation of uranium in natural near-surface sediment. Appl Environ Microbiol 71:1790-1797.
57. Thomas SH, Padilla-Crespo E, Jardine PM, Sanford RA, Loffler FE. 2009. Diversity and distribution of anaeromyxobacter strains in a uraniumcontaminated subsurface environment with a nonuniform groundwater flow. Appl Environ Microbiol 75:3679-3687.
58. Vrionis HA, Anderson RT, Ortiz-Bernad I, O'Neill KR, Resch CT, Peacock AD, Dayvault R, White DC, Long PE, Lovley DR. 2005. Microbiological and geochemical heterogeneity in an in situ uranium bioremediation field site. Appl Environ Microbiol 71:6308-6318.
59. Wall JD, Krumholz LR. 2006. Uranium reduction. Annu Rev Microbiol 60:149-166.
60. Wan J, Tokunaga TK, Kim Y, Brodie E, Daly R, Hazen TC, Firestone MK. 2008. Effects of organic carbon supply rates on uranium mobility in a previously bioreduced contaminated sediment. Environ Sci Technol 42:7573-7579.
61. White D, Davis WM, Nickels JS, King JD, Bobbie RJ. 1979. Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40:51-62.
62. White DC, Stair JO, Ringelberg DB. 1996. Quantitative comparisons of in situ microbial biodiversity by signature biomarker analysis. J Ind Microbiol 17:185-196.
63. Wu Q, Sanford RA, Loffler FE. 2006. Uranium(VI) reduction by Anaeromyxobacter dehalogenans strain 2CP-C. Appl Environ Microbiol 72:3608-3614.
64. Wu WM, Carley J, Luo J, Ginder-Vogel MA, Cardenas E, Leigh MB, Hwang C, Kelly SD, Ruan C, Wu L, Van Nostrand J, Gentry T, Lowe K, Mehlhorn T, Carroll S, Luo W, Fields MW, Gu B, Watson D, Kemner KM, Marsh T, Tiedje J, Zhou J, Fendorf S, Kitanidis PK, Jardine PM, Criddle CS. 2007. In situ bioreduction of uranium (VI) to submicromolar levels and reoxidation by dissolved oxygen. Environ Sci Technol 41:5716-5723.