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Uranium reduction and microbial community development in response to stimulation with different electron donors

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Abstract

Stimulating microbial reduction of soluble U(VI) to less soluble U(IV) shows promise as an in situ bioremediation strategy for uranium contaminated groundwater, but the optimal electron donors for promoting this process have yet to be identified. The purpose of this study was to better understand how the addition of various electron donors to uranium-contaminated subsurface sediments affected U(VI) reduction and the composition of the microbial community. The simple electron donors, acetate or lactate, or the more complex donors, hydrogen-release compound (HRC) or vegetable oil, were added to the sediments incubated in flow-through columns. The composition of the microbial communities was evaluated with quantitative PCR probing specific 16S rRNA genes and functional genes, phospholipid fatty acid analysis, and clone libraries. All the electron donors promoted U(VI) removal, even though the composition of the microbial communities was different with each donor. In general, the overall biomass, rather than the specific bacterial species, was the factor most related to U(VI) removal. Vegetable oil and HRC were more effective in stimulating U(VI) removal than acetate. These results suggest that the addition of more complex organic electron donors could be an excellent option for in situ bioremediation of uranium-contaminated groundwater.

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References

  • Anderson RT, Vrionis HA, Ortiz-bernad I, Resch CT, Long PE, Dayvault R, Karp K, Marutzky S, Metzler DR, Peacock AD, White DC, 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

    Article  PubMed  CAS  Google Scholar 

  • Araya R, Tani K, Takagi T, Yamaguchi N, Nasu M (2003) Bacterial activity and community composition in stream water and biofilm from an urban river determined by fluorescent in situ hybridization and DGGE analysis. FEMS Microbiol Ecol 43:111–119

    Article  PubMed  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1954) A rapid method of total lipid extraction and purification. Can J Biochem Phys 37:911–917

    Article  Google Scholar 

  • Borden RC (2007) Effective distribution of emulsified edible oil for enhanced anaerobic bioremediation. J Contam Hydrol 94:1–12

    Article  PubMed  CAS  Google Scholar 

  • Brümmer IH, Fehr W, Wagner-Döbler I (2000) Biofilm community structure in polluted rivers: abundance of dominant phylogenetic groups over a complete annual cycle. Appl Environ Microbiol 66:3078–3082

    Article  PubMed  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  PubMed  CAS  Google Scholar 

  • Edwards L, Kusel K, Drake H, Kostka J (2007) Electron flow in acidic subsurface sediments co-contaminated with nitrate and uranium. Geochim Cosmochim Ac 71:643–654

    Article  CAS  Google Scholar 

  • Esteve-Núñez A, Nunez C, Lovley DR (2004) Preferential reduction of Fe(III) over fumarate by Geobacter sulfurreducens. J Bacteriol 186:2897–2899

    Article  PubMed  Google Scholar 

  • Faybishenko B, Hazen TC, Long PE, Brodie EL, Conrad ME, Hubbard SS, Christensen JN, Joyner D (2008) In situ long-term reductive bioimmobilization of Cr(VI) in groundwater using hydrogen release compound. Environ Sci Technol 42:8478–8485

    Article  PubMed  CAS  Google Scholar 

  • Finneran KT, Anderson RT, Nevin KP, Lovley DR (2002) Potential for bioremediation of uranium-contaminated aquifers with microbial U(VI) reduction. Soil Sediment Contam 11:339–357

    Article  CAS  Google Scholar 

  • Gorby YA, Lovley DR (1992) Enzymatic uranium precipitation. Environ Sci Technol 26:205–207

    Article  CAS  Google Scholar 

  • Guckert JB, Antworth CP, Nichols PD, White DC (1985) Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Lett 31:147–158

    CAS  Google Scholar 

  • Haas JE, Trego DA (2001) A field application of Hydrogen-Releasing Compound (HRC (TM)) for the enhanced bioremediation of Methyl Tertiary Butyl Ether (MTBE). Soil Sediment Contam 10:555–575

    Article  CAS  Google Scholar 

  • Hazen TC, Tabak HH (2005) Developments in bioremediation of soils and sediments polluted with metals and radionuclides: 2. field research on bioremediation of metals and radionuclides. Rev Environ Sci Biotechnol 4:157–183

    Article  CAS  Google Scholar 

  • Holmes DE, Finneran KT, Neil RAO, 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

    Article  PubMed  CAS  Google Scholar 

  • Holmes DE, O’Neil RA, Vrionis HA, N’Guessan LA, Ortiz-Bernad I, Larrahondo MJ, Adams LA, Ward JA, Nicoll JS, Nevin KP, Chavan MA, Johnson JP, Long PE, Lovley DR (2007) Subsurface clade of Geobacteraceae that predominates in a diversity of Fe(III)-reducing subsurface environments. ISME J 1:663–677

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Junier P, Suvorova EI, Bernier-Latmani R (2010) Effect of competing electron acceptors on the reduction of U(VI) by Desulfotomaculum reducens. Geomicrobiol J 27:435–443

    Article  CAS  Google Scholar 

  • Karr EA, Sattley WM, Rice MR, Jung DO, Madigan MT, Achenbach LA (2005) Diversity and distribution of sulfate-reducing bacteria in permanently frozen Lake Fryxell, McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 71:6353–6359

    Article  PubMed  CAS  Google Scholar 

  • Komlos J, Kukkadapu RK, Zachara JM, Jaffe PR (2007) Biostimulation of iron reduction and subsequent oxidation of sediment containing Fe-silicates and Fe-oxides: Effect of redox cycling on Fe(III) bioreduction. Water Res 41:2996–3004

    Article  PubMed  CAS  Google Scholar 

  • Komlos J, Mishra B, Lanzirotti A, Myneni SCB, Jaffe PR (2008a) Real-time speciation of uranium during active bioremediation and U(IV) reoxidation. J Environ Eng 134:78–86

    Article  CAS  Google Scholar 

  • Komlos J, Moon HS, Jaffe PR (2008b) Effect of sulfate on the simultaneous bioreduction of iron and uranium. J Environ Qual 37:2058–2062

    Article  PubMed  CAS  Google Scholar 

  • Komlos J, Peacock AD, Kukkadapu R, Jaffe PR (2008c) Long-term dynamics of uranium reduction/reoxidation under low sulfate conditions. Geochim Cosmochim Ac 72:3603–3615

    Article  CAS  Google Scholar 

  • Kukkadapu RK, Zachara JM, Fredrickson JK, McKinley JP, Kennedy DW, Smith SC, Dong HL (2006) Reductive biotransformation of Fe in shale-limestone saprolite containing Fe(III) oxides and Fe(II)/Fe(III) phyllosilicates. Geochim Cosmochim Ac 70:3662–3676

    Article  CAS  Google Scholar 

  • Lack JG, Chaudhuri SK, Kelly SD, Kemner KM, O’Connor SM, Coates JD (2002) Immobilization of radionuclides and heavy metals through anaerobic bio-oxidation of Fe(II). Appl Environ Microbiol 68:2704–2710

    Article  PubMed  CAS  Google Scholar 

  • Li L, Steefel CI, Williams KH, Wilkins MJ, Hubbard SS (2009) Mineral transformation and biomass accumulation associated with uranium bioremediation at Rifle, Colorado. Environ Sci Technol 43:5429–5435

    Article  PubMed  CAS  Google Scholar 

  • Lindow NL, Borden RC (2005) Anaerobic bioremediation of acid mine drainage using emulsified soybean oil mine. Water Environ 24:199–208

    Article  CAS  Google Scholar 

  • Liu CX, 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

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JR, Macaskie LE (2000) Bioremediation of radionuclide-containing wastewaters. In: Lovley DR (ed) Environmental microbe-metal interactions. ASM Press, Washington, pp 277–327

    Google Scholar 

  • Long CM, Borden RC (2006) Enhanced reductive dechlorination in columns treated with edible oil emulsion. J Contam Hydrol 87:54–72

    Article  PubMed  CAS  Google Scholar 

  • Lovley DR (1995) Bioremediation of organic and metal contaminants with dissimilatory metal reduction. J Ind Microbiol 14:85–93

    Article  PubMed  CAS  Google Scholar 

  • Lovley DR, Phillips EJP (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540

    PubMed  CAS  Google Scholar 

  • Lovley DR, Phillips EJP (1992) Reduction of uranium by Desulfovibrio desulfuricans. Appl Environ Microbiol 58:850–856

    PubMed  CAS  Google Scholar 

  • Lovley DR, Phillips EJP, Gorby YA, Landa ER (1991) Microbial reduction of uranium. Nature 350:413–416

    Article  CAS  Google Scholar 

  • Lovley DR, Roden EE, Phillips EJP, Woodward JC (1993) Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Mar Geol 113:41–53

    Article  CAS  Google Scholar 

  • Luo WS, Wu WM, Yan TF, Criddle CS, Jardine PM, Zhou JZ, Gu BH (2007) Influence of bicarbonate, sulfate, and electron donors on biological reduction of uranium and microbial community composition. Appl Microbiol Biotechnol 77:713–721

    Article  PubMed  CAS  Google Scholar 

  • Madden AS, Palumbo AV, Ravel B, Vishnivetskaya TA, Phelps TJ, Schadt CW, Brandt CC (2008) Donor-dependent extent of uranium reduction for bioremediation of contaminated sediment microcosms. J Environ Qual 38:53–60

    Article  Google Scholar 

  • Marshall MJ, Dohnalkova AC, Kennedy DW, Plymale AE, Thomas SH, Loffler FE, Sanford RA, Zachara JM, Fredrickson JK, Beliaev AS (2009) Electron donor-dependent radionuclide reduction and nanoparticle formation by Anaeromyxobacter dehalogenans strain 2CP-C. Environ Microbiol 11:534–543

    Article  PubMed  CAS  Google Scholar 

  • Moller B, Obmer R, Howard BH, Gottsehalk G, Hippe H (1984) Sporomusa, a new genus of gram-negative anaerobic bacteria including Sporomusa sphaeroides spec nov and Sporomusa ovata spec nov. Arch Microbiol 139:388–396

    Article  Google Scholar 

  • Moon HS, Komlos J, Jaffe PR (2009) Biogenic U(IV) oxidation by dissolved oxygen and nitrate in sediment after prolonged U(VI)/Fe(III)/SO42- reduction. J Contam Hydrol 105:18–27

    Article  PubMed  CAS  Google Scholar 

  • Mouser PJ, N’Guessan AL, Elifantz H, Holmes DE, Williams KH, Wilkins MJ, Long PE, Lovley DR (2009) Influence of heterogeneous ammonium availability on bacterial community structure and the expression of nitrogen fixation and ammonium transporter genes during in situ bioremediation of uranium-contaminated groundwater. Environ Sci Technol 43:4386–4392

    Article  PubMed  CAS  Google Scholar 

  • N’Guessan AL, Vrionis HA, Resch CT, Long PE, Lovley DR (2008) Sustained removal of uranium from contaminated groundwater following stimulation of dissimilatory metal reduction. Environ Sci Technol 42:2999–3004

    Article  PubMed  Google Scholar 

  • Nevin KP, Finneran KT, Lovley DR (2003) Microorganisms associated with uranium bioremediation in a high-salinity subsurface sediment. Appl Environ Microbiol 69:3672–3675

    Article  PubMed  CAS  Google Scholar 

  • Prakash O, Gihring TM, Dalton DD, Chin KJ, Green SJ, Akob DM, Wanger G, Kostka JE (2010) Geobacter daltonii sp nov, an Fe(III)- and uranium(VI)-reducing bacterium isolated from a shallow subsurface exposed to mixed heavy metal and hydrocarbon contamination. Int J Syst Evol Microbial 60:546–553

    Article  CAS  Google Scholar 

  • Rubin MA, Leff LG (2007) Nutrients and other abiotic factors affecting bacterial communities in an Ohio River (USA). Microb Ecol 54:374–383

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Snoeyenbos-West OL, Nevin KP, Anderson RT, Lovley DR (2000) Enrichment of species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microb Ecol 39:153–167

    Article  PubMed  CAS  Google Scholar 

  • Stults JR, Snoeyenbos-West O, Methe B, Lovley DR, Chandler DP (2001) Application of the 5′ fluorogenic exonuclease assay (TaqMan) for quantitative ribosomal DNA and rRNA analysis in sediments. Appl Environ Microbiol 67:2781–2789

    Article  PubMed  CAS  Google Scholar 

  • Suzuki MT, Taylor LT, DeLong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Appl Environ Microbiol 66:4605–4614

    Article  PubMed  CAS  Google Scholar 

  • Suzuki Y, Kelly SD, Kemner KM, Banfield JF (2004) Enzymatic U(VI) reduction by Desulfosporosinus species. Radiochim Acta 92:11–16

    Article  CAS  Google Scholar 

  • Vrionis HA, Anderson RT, Ortiz-bernad I, Neill KRO, 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

    Article  PubMed  CAS  Google Scholar 

  • Wall JD, Krumholz LR (2006) Uranium reduction. Annu Rev Microbiol 60:149–166

    Article  PubMed  CAS  Google Scholar 

  • White DC, Ringelberg DB (1998) Signature lipid biomarker analysis. In: Burlage RS, Atlas R, Stahl D, Geesey G, Sayler G (eds) Techniques in microbial ecology. Oxford University Press, New York, pp 255–272

  • White DC, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 62:51–62

    Article  Google Scholar 

  • Williams KH, Long PE, Davis JA, Steefel CI, Wilkins MJ, N’Guessan AL, Yang L, Newcomer D, Spane FA, Kerkhof LJ, McGuiness L, Dayvault R, Lovley DR (2011) Acetate availability and its influence on sustainable bioremediation of uranium-contaminated groundwater. Geomicrobiol J (in press)

  • Wu WM, Carley J, Gentry T, Ginder-Vogel MA, Fienen M, Mehlhorn T, Yan H, Caroll S, Pace MN, Nyman J, Luo J, Gentile ME, Fields MW, Hickey RF, Gu BH, Watson D, Cirpka OA, Zhou JZ, Fendorf S, Kitanidis PK, Jardine PM, Criddle CS (2006) Pilot-scale in situ bioremedation of uranium in a highly contaminated aquifer. 2. Reduction of U(VI) and geochemical control of U(VI) bioavailability. Environ Sci Technol 40:3986–3995

    Article  PubMed  CAS  Google Scholar 

  • Wu WM, Carley J, Luo J, Ginder-Vogel MA, Cardenas E, Leigh MB, Hwang CC, Kelly SD, Ruan CM, Wu LY, Van Nostrand J, Gentry T, Lowe K, Mehlhorn T, Carroll S, Luo WS, Fields MW, Gu BH, Watson D, Kemner KM, Marsh T, Tiedje J, Zhou JZ, 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

    Article  PubMed  CAS  Google Scholar 

  • Yabusaki SB, Fang Y, Long PE, Resch CT, Peacock AD, Komlos J, Jaffe PR, Morrison SJ, Dayvault RD, White DC, Anderson RT (2007) Uranium removal from groundwater via in situ biostimulation: field-scale modeling of transport and biological processes. J Contam Hydrol 93:216–235

    Article  PubMed  CAS  Google Scholar 

  • Zhuang K, Izallalen M, Mouser P, Richter H, Risso C, Mahadevan R, Lovley DR (2011) Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments. ISME J 5:305–316

    Article  PubMed  Google Scholar 

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Acknowledgments

This research was funded by the Environmental Remediation Sciences Program (ERSP), Office of Biological and Environmental Research (OBER), U.S. Department of Energy (DOE), Pacific Northwest National Laboratory Project 51882 “The Rifle, Colorado Integrated Field Research Challenge Site (IFRC)”. Additional financial support for Dr. Moon was provided by Brain Korea 21 Project through the School of Earth and Environmental Sciences, Seoul National University in 2011.

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Correspondence to Peter R. Jaffe.

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Melissa Barlett and Hee Sun Moon have contributed equally to the study.

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Barlett, M., Moon, H.S., Peacock, A.A. et al. Uranium reduction and microbial community development in response to stimulation with different electron donors. Biodegradation 23, 535–546 (2012). https://doi.org/10.1007/s10532-011-9531-8

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  • DOI: https://doi.org/10.1007/s10532-011-9531-8

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