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Interaction of uranium (VI) with bacteria: potential applications in bioremediation of U contaminated oxic environments

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Abstract

Uranium and other metallic wastes released due to geochemical and several anthropogenic activities cause enormous damage to the environment. The fate and mobility of uranium (U) in the environment is affected by diverse microorganisms which interact through different mechanisms. Uranium at contaminated sites exists predominantly in two most common and stable valence states forms—the most oxidized valence state U(VI) exists as the highly soluble and toxic uranyl species (UO2 2+) while the reduced insoluble and less mobile, U(IV) is stable in the form of the mineral uraninite (UO2) under anoxic conditions. Reduced U(IV) species is less toxic and poorly soluble but it is liable to reoxidation and subsequent remobilization to soluble and more toxic U(VI) under oxic conditions. Fundamental understanding of nonreductive bacterial interaction mechanisms affecting the mobility and solubility of U(VI) in the environment is useful for developing suitable remediation and long-term management plan for U-contaminated sites. The present study gives an overview of various nonreductive bacterial interaction processes which affects the mobility and solubility of U(VI) in oxygenic environments.

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References

  • Aksu Z, Dönmez G (2000) The use of molasses in copper (II) containing wastewaters: effect on growth and copper(II) bioaccumulation properties of Kluveromyces marxianus. Process Biochem 36:451–458

    Article  CAS  Google Scholar 

  • Andres Y, MacCordick HJ, Hubert JC (1994) Binding sites of sorbed uranyl ion in the cell wall of Mycobacterium smegmatis. FEMS Microbiol Lett 115:27–32

    Article  CAS  Google Scholar 

  • Bargar JR, Reitmeyer R, Davis JA (1999) Spectroscopic confirmation of uranium(VI)-carbonato adsorption complexes on hematite. Environ Sci Technol 33:2481–2484

    Article  CAS  Google Scholar 

  • Bargar JR, Williams KH, Campbell KM, Long PE, Stubbs JE, Suvorova EI, Lezama-Pacheco JS, Alessi DS, Stylo M, Webb SM, Davis JA, Giammar DE, Blue LY, Bernier-Latmani R (2013) Uranium redox transition pathways in acetate-amended sediments. Proc Natl Acad Sci 110:4506–4511

    Article  CAS  Google Scholar 

  • Barkleit A, Foerstendorf H, Li B, Rossberg A, Moll H, Bernhard G (2011) Coordination of uranium(VI) with functional groups of bacterial lipopolysaccharide studied by EXAFS and FT-IR spectroscopy. Dalton Trans 40(38):9868–9876

    Article  CAS  Google Scholar 

  • Beazley MJ, Martinez RJ, Sobecky PA, Webb SM, Taillefert M (2007) Uranium biomineralization as a result of bacterial phosphatase activity: insights from bacterial isolates from a contaminated subsurface. Environ Sci Technol 41:5701–5707

    Article  CAS  Google Scholar 

  • Beazley MJ, Martinez RJ, Sobecky PA, Webb SM, Taillefert M (2009) Nonreductive biomineralization of uranium(VI) phosphate via microbial phosphatase activity in anaerobic conditions. Geomicrobiol J 26:431–441

    Article  CAS  Google Scholar 

  • Beazley MJ, Martinez RJ, Webb SM, Sobecky PA, Taillefert M (2011) The effect of pH and natural microbial phosphatase activity on the speciation of uranium in subsurface soils. Geochim Cosmochim Acta 75:5648–5663

    Article  CAS  Google Scholar 

  • Beech IB, Cheung CWS (1995) Interactions of exopolymers produced by sulphate-reducing bacteria with metal ions. Int Biodeterior Biodegrad 35:59–72

    Article  CAS  Google Scholar 

  • Birch L, Bachofen R (1990) Complexing agents from microorganisms. Experientia 46:827–834

    Article  CAS  Google Scholar 

  • Brown CF, Um W, Serne RJ (2008) Uranium contamination in the 300 area: emergent data and their impact on the source term conceptual model. PNNL-17793, Pacific Northwest National Laboratory, Richland, WA

  • Cardenas E, Wu WM, Leigh MB, Carley J, Carroll S, Gentry T, Luo J, Watson D, Gu B, Ginder-Vogel M, 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. doi:10.1128/AEM.02308-07

    Article  CAS  Google Scholar 

  • Chojnacka K (2010) Biosorption and bioaccumulation-the prospects for practical applications. Environ Int 36:299–307

    Article  CAS  Google Scholar 

  • Choudhary S, Sar P (2011) Uranium biomineralization by a metal resistant Pseudomonas aeruginosa strain isolated from contaminated mine waste. J Hazard Mater 186:336–343

    Article  CAS  Google Scholar 

  • Converse BJ, Wu T, Findlay RH, Roden EE (2013) U(VI) reduction in sulfate-reducing subsurface sediments amended with ethanol or acetate. Appl Environ Microbiol 79:4173–4177

    Article  CAS  Google Scholar 

  • Dhal PK, Sar P (2014) Microbial communities in uranium mine tailings and mine water sediment from Jaduguda U mine, India: A culture independent analysis. J Environ Sci Health A Tox Hazard Subst Environ Eng 49(6):694–709

  • Fein J, Yee N, Davis TA (1997) A chemical equilibrium model for metal adsorption onto bacterial surface. Geochim Cosmochim Acta 61:3319–3328

    Article  CAS  Google Scholar 

  • Fowle DA, Fein JB, Martin AM (2000) Experimental study of uranyl adsorption onto Bacillus subtilis. Environ Sci Technol 34:3737–3741

    Article  CAS  Google Scholar 

  • Francis AJ, Gillow JB, Dodge CJ, Harris R, Harris R, Beveridge TJ, Papenguth HW (2004) Uranium association with halophilic and non-halophilic bacteria and archaea. Radiochim Acta 92:481–488

    Article  CAS  Google Scholar 

  • Gadd GM (1992) Metals and microorganisms: a problem of definition. FEMS Microbiol Lett 79:197–203

    Article  Google Scholar 

  • Gadd GM (2004) Microbial influence on metal mobility and application for bioremediation. Geoderma 122:109–119

    Article  CAS  Google Scholar 

  • Gavrilescu M, Pavel LV, Cretescu I (2009) Characterization and remediation of soils contaminated with uranium. J Hazard Mater 163:475–510

    Article  CAS  Google Scholar 

  • Gorman-Lewis D, Elias PE, Fein JB (2005) Adsorption of aqueous uranyl complexes onto Bacillus subtilis cells. Environ Sci Technol 39:4906–4912

    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 

  • Islam E, Paul D, Sar P (2014) Microbial diversity in Uranium deposits from Jaduguda and Bagjata Uranium mines, India as revealed by clone library and denaturing gradient gel electrophoresis analyses. Geomicrobiol J. doi:10.1080/01490451.2014.907375

  • Kazy SK, Sar P, Singh SP, Sen AK, D’Souza SF (2002) Extracellular polysaccharides of a copper-sensitive and a copper-resistant Pseudomonas aeruginosa strain: synthesis, chemical nature and copper binding. World J Microbiol Biotechnol 18:583–588

    Article  CAS  Google Scholar 

  • Kazy SK, D’Souza SF, Sar P (2009) Uranium and thorium sequestration by a Pseudomonas sp.: mechanism and chemical characterization. J Hazard Mater 163:65–72

    Article  CAS  Google Scholar 

  • Keasling JD, Hupf GA (1996) Genetic manipulation of polyphosphate metabolism affects cadmium tolerance in Escherichia coli. Appl Environ Microbiol 62:743–746

    CAS  Google Scholar 

  • Kelly SD, Kemner KM, Fein JB, Fowle DA, Boyanov MI, Bunker BA, Yee N (2002) X-ray absorption fine structure determination of pH dependent U-bacterial cell wall interactions. Geochim Cosmochim Acta 65:3855–3871

    Article  Google Scholar 

  • Koban A, Geipel G, Roßberg A, Bernhard G (2004) Uranyl (VI) complexes with sugar phosphates in aqueous solution. Radiochim Acta 92:903–908

    Article  CAS  Google Scholar 

  • Kumar R, Nongkhlaw M, Acharya C, Joshi SR (2013) Uranium (U)-tolerant bacterial diversity from U ore deposit of Domiasiat in North-East India and its prospective utilisation in bioremediation. Microbes Environ 28(1):33–41

  • Lederer FL, Weinert U, Günther TJ, Raff J, Weiß S, Pollmann K (2013) Identification of multiple putative S-layer genes partly expressed by Lysinibacillus sphaericus JG-B53. Microbiology 159:1097–1108

    Article  CAS  Google Scholar 

  • Llorens I, Untereiner G, Jaillard D, Gouget B, Chapon V, Carriere M (2012) Uranium interaction with two multi-resistant environmental bacteria: Cupriavidus metallidurans CH34 and Rhodopseudomonas palustris. PLoS ONE 7(12):e51783

    Article  CAS  Google Scholar 

  • Lloyd JR, Macaskie LE (2000) Bioremediation of radionuclide containing wastewaters. In: Lovely DR (ed) Environmental metal microbe interaction. American Society of Microbiology, Washington, pp 227–327

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Luo W, Gu B (2011) Dissolution of uranium-bearing minerals and mobilization of uranium by organic ligands in a biologically reduced sediment. Environ Sci Technol 45(7):2994–2999

    Article  CAS  Google Scholar 

  • Lütke L, Moll H, Bernhard G (2012) Insights into the uranium(VI) speciation with Pseudomonas fluorescens on a molecular level. Dalton Trans 41(43):13370–13378

    Article  Google Scholar 

  • Macaskie LE, Empson RM, Cheetham AK, Grey CP, Skarnulis AJ (1992) Uranium bioaccumulation by a Citrobacter sp. as a result of enzymically mediated growth of polycrystalline HUO2PO4. Science 257:782–784

    Article  CAS  Google Scholar 

  • Macaskie LE, Bonthrone KM, Rouch DA (1994) Phosphatase-mediated heavy metal accumulation by a Citrobacter sp. and related enterobacteria. FEMS Microbiol Lett 121:141–146

    Article  CAS  Google Scholar 

  • Martinez RJ, Beazley MJ, Taillefert M, Arakaki AK, Skolnick J, Sobecky PA (2007) Aerobic uranium (VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide-and metal-contaminated subsurface soils. Environ Microbiol 9:3122–3133

    Article  CAS  Google Scholar 

  • Meinrath A, Schneider P, Meinrath G (2003) Uranium ores and depleted uranium in the environment, with a reference to uranium in the biosphere from the Erzgebirge/Sachsen, Germany. J Environ Radioact 64:175–193

    Article  CAS  Google Scholar 

  • Merroun ML, Selenska-Pobell S (2008) Bacterial interactions with uranium: an environmental perspective. J Contam Hydrol 102:285–295

    Article  CAS  Google Scholar 

  • Merroun ML, Geipel G, Nicolai R, Heise KH, Selenska-Pobell S (2003) Complexation of uranium (VI) by three eco-types of Acidithiobacillus ferrooxidans studied using time-resolved laser-induced fluorescence spectroscopy and infrared spectroscopy. Biometals 16:331–339

    Article  CAS  Google Scholar 

  • Merroun ML, Nedelkova M, Rossberg A, Hennig C, Selenska-Pobell S (2006) Interaction mechanisms of bacterial strains isolated from extreme habitats with uranium. Radiochim Acta 94:723–729

    Article  CAS  Google Scholar 

  • Mondani L, Piette L, Christen R, Bachar D, Berthomieu C, Chapon V (2013) Microbacterium lemovicicum sp. nov., a bacterium isolated from a natural uranium-rich soil. Int J Syst Evol Microbiol 63(Pt 7):2600–2606

    Article  CAS  Google Scholar 

  • Nakajima A, Tsuruta T (2004) Competitive biosorption of thorium and uranium by Micrococcus luteus. J Radioanal Nucl Chem 260:13–18

    Article  CAS  Google Scholar 

  • Nedelkova M, Merroun ML, Rossberg A, Hennig C, Selenska-Pobell S (2007) Microbacterium isolates from the vicinity of a radioactive waste depository and their interactions with uranium. FEMS Microbiol Ecol 59:694–705

    Article  CAS  Google Scholar 

  • Newsome L, Morris K, Lloyd JR (2014) The biogeochemistry and bioremediation of uranium and other priority radionuclides. Chem Geol 363:164–184

    Article  CAS  Google Scholar 

  • Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750

    Article  CAS  Google Scholar 

  • 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 co-contaminated with uranium and nitrate. Appl Environ Microbiol 70:4911–4920

    Article  CAS  Google Scholar 

  • Orellana R, Leavitt JJ, Comolli LR, Csencsits R, Janot N, Flanagan KA, Gray AS, Leang C, Izallalen M, Mester T, Lovley DR (2013) U(VI) reduction by diverse outer surface c-type cytochromes of geobacter sulfurreducens. Appl Environ Microbiol 79:6369–6374

    Article  CAS  Google Scholar 

  • Panak PJ, Knopp R, Booth CH, Nitsche H (2002) Spectroscopic studies on the interaction of U(VI) with Bacillus sphaericus. Radiochim Acta 90:779–783

    CAS  Google Scholar 

  • Rashmi V, Shylajanaciyar M, Rajalakshmi R, D’Souza SF, Prabaharan D, Uma L (2013) Siderophore mediated uranium sequestration by marine cyanobacterium Synechococcus elongatus BDU 130911. Bioresour Technol 130:204–210

    Article  CAS  Google Scholar 

  • Reeder RJ, Nugent M, Tait CD, Morris DE, Heald SM, Beck KM, Hess WP, Lanzirotti A (2001) Coprecipitation of uranium (VI) with calcite: XAFS, micro-XAS, and luminescence characterization. Geochim Cosmoschim Acta 65:3491–3503

    Article  CAS  Google Scholar 

  • Renninger N, Knopp R, Nitsche H, Clark DS, Keasling JD (2004) Uranyl precipitation by Pseudomonas aeruginosa via controlled polyphosphate metabolism. Appl Environ Microbiol 70:7404–7412

    Article  CAS  Google Scholar 

  • Renshaw JC, Robson GD, Trinci APJ, Wiebe MG, Livens FR, Collison D, Taylor RJ (2002) Fungal siderophores: structures, functions and applications. Mycol Res 106:1123–1142

    Article  CAS  Google Scholar 

  • Salome KR, Green SJ, Beazley MJ, Webb SM, Kostka JE, Taillefert M (2013) The role of anaerobic respiration in the immobilization of uranium through biomineralization of phosphate minerals. Geochim Cosmochim Acta 106:344–363

    Article  CAS  Google Scholar 

  • Selenska-Pobell S, Panak P, Miteva V, Boudakov I, Bernhard G, Nitsche H (1999) Selective accumulation of heavy metals by three indigeneous Bacillus strains, B. cereus, B. megaterium and B. sphaericus, from drain waters of a uranium waste pile. FEMS Microbiol Ecol 29:59–67

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shelobolina ES, Konishi H, Xu HF, Roden EE (2009) U(VI) sequestration in hydroxyapatite produced by microbial glycerol 3-phosphate metabolism. Appl Environ Microbiol 75:5773–5778

    Article  CAS  Google Scholar 

  • Singh G, Şengör SS, Bhalla A, Kumar S, De J, Stewart B, Spycher N, Ginn TM, Peyton BM, Sani RK (2014) Reoxidation of biogenic reduced uranium: a challenge towards bioremediation. Crit Rev Environ Sci Tech 44:391–415

    Article  CAS  Google Scholar 

  • Sousa T, Chung AP, Pereira A, Piedade AP, Morais PV (2013) Aerobic uranium immobilization by Rhodanobacter A2-61 through formation of intracellular uranium–phosphate complexes. Metallomics 5:390–397

    Article  CAS  Google Scholar 

  • Suzuki SY, Banfield JF (1999) Geomicrobiology of uranium. In: Burns PC, Finch R (eds) Uranium: mineralogy, geochemistry and the environment, vol. 38. Mineralogical Society of America, Washington, pp 393–432

  • Templeton A, Knowles E (2009) Microbial transformations of minerals and metals: recent advances in geomicrobiology derived from synchrotron-based X-ray spectroscopy and X-ray microscopy. Annu Rev Earth Planet Sci 37:391

    Article  Google Scholar 

  • Todorov PT, Ilieva EN (2006) Contamination with uranium from natural and anthropological sources. Rom J Phys 51:27–34

    CAS  Google Scholar 

  • Van Veen HW, Abee T, Kortstee GJJ, Konings WN, Zehnder AJB (1993) Characterization of two phosphate transport systems in Acinetobacter johnsonii 210A. J Bacteriol 175:200–206

    Google Scholar 

  • Yong P, Macaskie LE (1995) Role of citrate as a complexing ligand which permits enzymically-mediated uranyl ion bioaccumulation. Bull Environ Contam Toxicol 54:892–899

    Article  CAS  Google Scholar 

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Choudhary, S., Sar, P. Interaction of uranium (VI) with bacteria: potential applications in bioremediation of U contaminated oxic environments. Rev Environ Sci Biotechnol 14, 347–355 (2015). https://doi.org/10.1007/s11157-015-9366-6

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