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Bacterial Communities of Uranium-Contaminated Tailing Ponds and Their Interactions with Different Heavy Metals

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Advances in Soil Microbiology: Recent Trends and Future Prospects

Part of the book series: Microorganisms for Sustainability ((MICRO,volume 3))

Abstract

Discharge of uranium (U) tailings and contaminant effluents from uranium ore extraction sites creates huge burdens of anthropogenic radioactivity and greatly alters the ecosystem. Remediating the environment from these contaminations thus becomes a huge responsibility of the industry. Microbe-based bioremediation has emerged as a potential alternative to hazardous mine waste management as well as removal of toxic contaminants efficiently from the environment. In order to formulate the bioremediation strategies effectively, it is essential to understand the inhabitant microbial community structure of mine sites and their metabolic role as related to those sites. In addition, deciphering microbial communities also helps us to understand the responsible biogeochemical cycling and food web dynamics of such sites. Advancement in different techniques that includes high-throughput DNA sequencing and different “omic” tools can provide details of microbial communities and their metabolic activity in contaminated environments. The present chapter will describe both culturable and unculturable microbial diversity, dynamics within the uranium tailing pond, and radionuclide-contaminated environment and their interaction with other heavy metals including uranium.

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References

  • Akob DM, Mills HJ, Kostka JE (2007) Metabolically active microbial communities in uranium-contaminated subsurface sediments. FEMS Microbiol Ecol 59:95–107

    Article  CAS  PubMed  Google Scholar 

  • Akob DM, Kerkhof L, Küsel K, Watson DB, Palumbo AV, Kostka JE (2011) Linking specific heterotrophic bacterial populations to bioreduction of uranium and nitrate in contaminated subsurface sediments by using stable isotope probing. Appl Environ Microbiol 77(22):8197–8200

    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  PubMed  Google Scholar 

  • Andres Y, Redercher S, Gerente C, Thouand G (2001) Contribution of biosorption of radionuclides in the environment. J Radioanal Nucl Chem 247:89–93

    Article  CAS  Google Scholar 

  • Antunes SC, Pereira R, Marques SM, Castro BB, Gonçalves F (2011) Impaired microbial activity caused by metal pollution: a field study in a deactivated uranium mining area. Sci Total Environ 410:87–95

    Article  PubMed  CAS  Google Scholar 

  • Barkay T, Schaefer J (2001) Metal and radionuclide bioremediation: issues, considerations and potentials. Curr Opin Microbiol 4:318–323

    Article  CAS  PubMed  Google Scholar 

  • Barns SM, Cain EC, Sommerville L, Kuske CR (2007) Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73:3113–3116

    Article  CAS  PubMed  PubMed Central  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  PubMed  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 

  • Beller HR (2005) Anaerobic, nitrate-dependent oxidation of U(IV) oxide minerals by the chemolithoautotrophic bacterium Thiobacillus denitrificans. Appl Environ Microbiol 71:2170–2174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beyenal H, Sani RK, Peyton BM, Dohnalkova AC, Amonette JE, Lewandowski Z (2004) Uranium immobilization by sulfate-reducing biofilms. Sci Total Environ 38:2067–2074

    Article  CAS  Google Scholar 

  • Bondici VF, Lawrence JR, Khan NH, Hill JE, Yergeau E, Wolfaardt GM, Warner J, Korber DR (2013) Microbial communities in low permeability, high pH uranium mine tailings: characterization and potential effects. J Appl Microbiol 114:1671–1686

    Article  CAS  PubMed  Google Scholar 

  • Bosecker K (1997) Bioleaching: metal solubilization by microorganisms. FEMS Microbiol Rev 20:591–604

    Article  CAS  Google Scholar 

  • Boswell CD, Dick RE, Macaskie LE (1999) The effect of heavy metals and other environmental conditions on the anaerobic phosphate metabolism of Acinetobacter johnsonii. Microbiology 145:1711–1720

    Article  CAS  PubMed  Google Scholar 

  • Brodie EL, DeSantis TZ, Joyner DC, Baek SM, Larsen JT, Andersen GL, Hazen TC, Richardson PM, Herman DJ, Tokunaga TK, Wan JM, Firestone MK (2006) Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl Environ Microbiol 72:6288–6298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brzoska RM, Bollmann A (2016) The long-term effect of uranium and pH on the community composition of an artificial consortium. FEMS Microbiol Ecol 92(1)

    Google Scholar 

  • Cardenas E, Wu WM, Leigh MB, Carley J, Carroll S, Gentry, Luo TJ, Watson D, Gu B, Ginder-Vogel M, Kitanidis PK, Jardine PM, Zhou J, Criddle CS, Marsh TL, Tiedje JA (2008) Microbial communities in contaminated sediments, associated with bioremediation of uranium to submicromolar levels. Appl Environ Microbiol 74:3718–3729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cerdá J, González S, Ríos JM, Quintana T (1993) Uranium concentrates bioproduction in Spain: a case study. FEMS Microbiol Rev 11:253–259

    Article  Google Scholar 

  • Chang YJ, Peacock AD, Long PE, Stephen JR, McKinley JP, Macnaughton SJ, Hussain AKA, Saxton M, White DC (2001) Diversity and characterization of sulfate-reducing bacteria in groundwater at a uranium mill tailings site. Appl Environ Microbiol 67:3149–3160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapon V, Piette L, Berthomieu C, Vesvres MH, Le Marrec C, Coppin L, Février L, Martin-Garin A, Sergean TC (2012) Microbial diversity in contaminated soils along the T22 trench of the Chernobyl experimental platform. Appl Geochem 27:1375–1383

    Article  CAS  Google Scholar 

  • Cho K, Zholi A, Frabutt D, Flood M, Floyd D, Tiquia SM (2012) Linking bacterial diversity and geochemistry of uranium-contaminated groundwater. Environ Technol 33:1629–1640

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Choudhary S, Sar P (2009) Characterization of a metal resistant Pseudomonas sp. isolated from uranium mine for its potential in heavy metal (Ni2+, Co2+, Cu2+, and Cd2+) sequestration. Bioresour Technol 100:2482–2492

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Choudhary S, Sar P (2011b) Identification and characterization of uranium accumulation potential of a uranium mine isolated Pseudomonas strain. W J Microbiol Biotechnol. https://doi.org/10.1007/s11274-010-0637-7

  • Choudhary S, Sar P (2011c) Identification and characterization of uranium accumulation potential of a uranium mine isolated Pseudomonas strain. World J Microbiol Biotechnol 27:1795–1801

    Article  CAS  Google Scholar 

  • Choudhary S, Sar P (2015) Interaction of uranium (VI) with bacteria: potential applications in bioremediation of U contaminated oxic environments. Rev Environ Sci Biotechnol 14:347–355

    Article  CAS  Google Scholar 

  • Choudhary S, Islam E, Kazy SK, Sar P (2012) Uranium and other heavy metal resistance and accumulation in bacteria isolated from uranium mine wastes. J Environ Sci Health Part A 47:622–637

    Article  CAS  Google Scholar 

  • Chourey K, Nissen S, Vishnivetskaya T, Shah M, Pfiffner S, Hettich RL, Löffler FE (2013) Environmental proteomics reveals early microbial community responses to biostimulation at a uranium- and nitrate-contaminated site. Proteomics 13(18–19):2921–2930

    CAS  PubMed  Google Scholar 

  • Coates JD, Bhupathiraju VK, Achenbach LA, McInerney MJ, Lovley DR (2001) Geobacter hydrogenophilus and Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe(III)-reducers. Int J Syst Evol Microbiol 51:581–588

    Article  CAS  PubMed  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 Part A 49:694–709

    Article  CAS  Google Scholar 

  • Dhal PK, Islam E, Kazy SK, Sar P (2011) Culture independent molecular analysis of bacterial diversity in uranium -ore/-mine waste contaminated and non-contaminated sites from uranium mines. 3 Biotech 1:261–272

    Article  PubMed  PubMed Central  Google Scholar 

  • Douglas S, Beveridge TJ (1998) Mineral formation by bacteria in natural microbial communities. FEMS Microbiol Rev 26:79–88

    Article  CAS  Google Scholar 

  • Elias DA, Krumholz LR, Wong D, Long PE, Suflita JM (2003) Characterization of microbial activities and U reduction in a shallow aquifer contaminated by uranium mill tailings. Microb Ecol 46:83–91

    Article  CAS  PubMed  Google Scholar 

  • Fields MW, Yan T, Rhee SK, Carroll SL, Jardine PM, Watson DB, Criddle CS, Zhou J (2005) Impacts on microbial communities and cultivable isolates from groundwater contaminated with high levels of nitric acid-uranium waste. FEMS Microbiol Ecol 53:417–428

    Article  CAS  PubMed  Google Scholar 

  • Fletcher KE, Boyanov MI, Thomas SH, Wu Q, Kemner KM, Löffler FE (2010) U(VI) reduction to mononuclear U(IV) by desulfitobacterium species. Environ Sci Technol 44:4705–4709

    Article  CAS  PubMed  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 

  • Francis AJ, Dodge CJ, Gillow JB (2008) Reductive Dissolution of Pu(IV) by Clostridium sp. under anaerobic conditions. Environ Sci Technol 42:2355–2360

    Article  CAS  PubMed  Google Scholar 

  • Fredrickson JK, Zachara JM, Balkwill DL, Kennedy D, Li SM, Kostandarithes HM, Daly MJ, Romine MF, Brockman FJ (2004) Geomicrobiology of high-level nuclear waste-contaminated vadose sediments at the hanford site, Washington state. Appl Environ Microbiol 70:4230–4241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuchs T, Huber H, Teiner K, Burggraf S, Stetter KO (1995) Metallosphaera prunae, sp. nov., a novel metal-mobilizing, isolated from a uranium mine in Germany. Syst Appl Microbiol 18:560–566

    Article  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 

  • Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643

    Article  CAS  PubMed  Google Scholar 

  • Geissler A (2007) Prokaryotic microorganisms in uranium mining waste piles and their interactions with uranium and other heavy metals. PhD Thesis, TU Bergakademie Freiberg, Freiberg

    Google Scholar 

  • Geissler A, Selenska-Pobell S (2005) Addition of U(VI) to a uranium mining waste sample and resulting changes in the indigenous bacterial community. Geobiology 3:275–285

    Article  CAS  Google Scholar 

  • Goodman AE, Khalid AM, Ralph BJ (1981) Microbial ecology of Rum Jungle I; environmental study of sulphidic overburden dumps, experimental heap leach piles and tailings dam area. Australian Atomic Energy Commission, Report AAEC/E531, Australia

    Google Scholar 

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

    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  PubMed  Google Scholar 

  • Green SJ, Prakash O, Jasrotia P, Overholt WA, Cardenas E, Hubbard D, Tiedje JM, Watson DB, Schadt CW, Brooks SC, Kostka JE (2012) Denitrifying bacteria from the genus Rhodanobacter dominate bacterial communities in the highly contaminated subsurface of a nuclear legacy waste site. Appl Environ Microbiol 78:1039–1047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hafez M, Ibrahim M, Abdel-Razek A, Abu-Shady M (2002) Biosorption of some ions on different bacterial species from aqueous and radioactive waste solutions. J Radioanal Nucl Chem 252:179–185

    Article  CAS  Google Scholar 

  • Hemme CL, Deng Y, Gentry TJ, Fields MW, Wu L, Barua S, Barry K, Tringe SG, Watson DB, He Z, Hazen TC, Tiedje JM, Rubin EM, Zhou J (2010) Metagenomic insights into evolution of a heavy metal-contaminated groundwater microbial community. ISME J 4:660–672

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Islam E, Sar P (2011) Culture-dependent and -independent molecular analysis of the bacterial community within uranium ore. J Basic Microbiol 4:372–384

    Article  CAS  Google Scholar 

  • Islam E, Sar P (2016) Diversity, metal resistance and uranium sequestration abilities of bacteria from uranium ore deposit in deep earth stratum. Ecotoxicol Environ Saf 127:12–21

    Article  CAS  PubMed  Google Scholar 

  • Islam E, Dhal PK, Sufia KK, Sar P (2011) Molecular analysis of bacterial communities in uranium ores and surrounding soils from Banduhurang open cast uranium mine, India: a comparative study. J Environ Sci Health Part A 46:271–280

    Article  CAS  Google Scholar 

  • Ivanova IA, Stephen JR, Chang Y-J, Brüggemann J, Long PE, McKinley JP, Kowalschuk GA, White DC, Macnaughton SJ (2000) A survey of 16S rRNA and amoA genes related to autotrophic ammonia-oxidizing bacteria of the β-subdivision of the class proteobacteria in contaminated groundwater. Can J Microbiol 46:1012–1020

    Article  CAS  PubMed  Google Scholar 

  • Jroundi F, Merroun ML, Arias JM, Rossberg A, Selenska-Pobell S, González-Muñoz MT (2007) Spectroscopic and microscopic characterization of uranium biomineralization in Myxococcus xanthus. Geomicrobiol J 24:441–449

    Article  CAS  Google Scholar 

  • Kashefi K, Lovely DR (2000) Reduction of Fe(III), Mn(IV), and toxic metals at 100 °C by Pyrobaculum islandicum. Appl Environ Microbiol 66:1050–1056

    Article  CAS  PubMed  PubMed Central  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  PubMed  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 

  • Kenarova A, Radeva G, Traykov I, Boteva S (2014) Community level physiological profiles of bacterial communities inhabiting uranium mining impacted sites. Ecotox Environ Safe 100:226–232

    Article  CAS  Google Scholar 

  • Khan NH, Bondici VF, Medihala PG, Lawrence JR, Wolfaardt GM, Warner J, Korber DR (2013) Bacterial diversity and composition of an alkaline uranium mine tailings-water interface. J Microbiol 51:558–569

    Article  CAS  PubMed  Google Scholar 

  • Kieft TL, Fredrickson JK, Onstott TC, Gorby YA, Kostandarithes HM, Bailey TJ, Kennedy DW, Li SW, Plymale AE, Spadoni CM, Gray MS (1999) Dissimilatory reduction of Fe(III) and other electron acceptors by a Thermus isolate. Appl Environ Microbiol 65:1214–1421

    CAS  PubMed  PubMed Central  Google Scholar 

  • Knopp R, Panak PJ, Wray LA, Renninger NS, Keasling JD, Nitsche H (2003) Laser spectroscopic studies of interactions of UVI with bacterial phosphate species. Chem Eur J 9:2812–2818

    Article  CAS  PubMed  Google Scholar 

  • Konopka A, Plymale AE, Carvajal DA, Lin XJ, Mckinley JP (2013) Environmental controls on the activity of aquifer microbial communities in the 300 Area of the Hanford site. Microb Ecol 66:889–896

    Article  CAS  PubMed  Google Scholar 

  • Kotelnikova S, Macario AJL, Pedersen K (1998) Methanobacterium subterraneum sp. nov., a new alkaliphilic, eurythermic and halotolerant methanogen isolated from deep granitic groundwater. Int J Syst Evol Microbiol 48:357–367

    Google Scholar 

  • Krueger S, Olson GJ, Johnsonbaugh D, Beveridge TJ (1993) Characterization of the binding of gallium, platinum, and uranium to Pseudomonas fluorescens by small-angle X-Ray scattering and transmission electron microscopy. Appl Environ Microbiol 59:4056–4064

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Lack J, Chaudhuri S, Kelly S, Kemner K, O´Connor S, Coates J (2002) Immobilization of radionuclides and heavy metals through anaerobic bio-oxidation of Fe(II). Appl Environ Microbiol 68:2704–2710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landa ER (2005) In: Laskin AI, Bennett JW, Gadd GM (eds) Microbial biogeochemistry of uranium mill tailings advances in applied microbiology, vol 57. Academic Press, Burlington, pp 113–130

    Google Scholar 

  • Langley S, Beveridge TJ (1999) Effect of O-side-chain lipopolysaccharide chemistry on metal binding. Appl Environ Microbiol 65:489–498

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leigh MB, Wu W, Cardenas E, Uhlik O, Carroll S, Gentry T, Marsh TL, Zhou J, Jardine P, Criddle CS, Tiedje JM (2014) Microbial communities biostimulated by ethanol during uranium (VI) bioremediation in contaminated sediment as shown by stable isotope probing. Front Environ Sci Eng 2015(9):453–464

    Google Scholar 

  • Lloyd J, Gadd G (2011) The geomicrobiology of radionuclides. Geomicrobiol J 28:383–386

    Article  CAS  Google Scholar 

  • Lloyd JR, Renshaw JC (2005) Microbial transformations of radionuclides: fundamental mechanisms and biogeochemical implication. Met Ions Biol Syst 44:205–240

    CAS  PubMed  Google Scholar 

  • Lovley D (1993) Dissimilatory metal reduction. Annu Rev Microbiol 47:263–290

    Article  CAS  PubMed  Google Scholar 

  • Lovley DR (2003) Cleaning up with genomics: applying molecular biology to bioremediation. Nat Rev Microbiol 1:35–44

    Article  CAS  PubMed  Google Scholar 

  • Lovley DR, Coates JD (1997) Bioremediation of metal contamination. Curr Opin Biotechnol 8:285–289

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Maleke M, Williams P, Castillo J, Botes E, Ojo A, DeFlaun M, van Heerden E (2014) Optimization of a bioremediation system of soluble uranium based on the biostimulation of an indigenous bacterial community. Environ Sci Pollut Res 22:8442–8450

    Article  CAS  Google Scholar 

  • Malekzadeh F, Farazmand A, Ghafourtian H, Shahamat M, Levin M, Colwell RR (2002) Uranium accumulation by a bacterium isolated from electroplating effluent. World J Microbiol Biotechnol 18:295–302

    Article  CAS  Google Scholar 

  • Marsili E, Beyenal H, Di Palma L, Merli C, Dohnalkova A, Amonette JE, Lewandowski Z (2007) Uranium immobilization by sulfate-reducing biofilms grown on hematite, dolomite, and calcite. Environ Sci Technol 41:8349–8354

    Article  CAS  PubMed  Google Scholar 

  • Martinez RJ, Wang Y, Raimondo MA, Coombs JM, Barkay T, Sobecky PA (2006) Horizontal gene transfer of PIB-type ATPases among bacteria isolated from radionuclide-and metal-contaminated subsurface soils. Appl Environ Microbiol 72:3111–3118

    Article  CAS  PubMed  PubMed Central  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  PubMed  Google Scholar 

  • McLean J, Beveridge TJ (2001) Chromate reduction by a Pseudomonad isolated from a site contaminated with chromated copper arsenate. Appl Environ Microbiol 67:1076–1084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merroun ML, Selenska-Pobell S (2001) Interactions of three eco-types of Acidithiobacillus ferrooxidans with U(VI). Biometals 14:171–179

    Article  CAS  PubMed  Google Scholar 

  • Merroun ML, Selenska-Pobell S (2008) Bacterial interactions with uranium: an environmental perspective. J Contam Hydrol 102:285–229

    Article  CAS  PubMed  Google Scholar 

  • Merroun ML, Hennig C, Rossberg A, Geipel G, Reich T, Selenska-Pobell S (2002) Molecular and atomic analysis of the uranium complexes formed by three ecotypes of Acidithiobacillus ferrooxidans. Biochem Sc Trans 30:669–672

    Article  CAS  Google Scholar 

  • Merroun ML, Hennig C, Rossberg A, Reich T, Selenska-Pobell S (2003) Characterization of U(VI)-Acidithiobacillus ferrooxidans complexes using EXAFS, transmission electron microscopy, and energy-dispersive X-ray analysis. Radiochim Acta 91:583–592

    Article  CAS  Google Scholar 

  • Merroun ML, Raff J, Rossberg A, Hennig C, Reich T, Selenska-Pobell S (2005) Complexation of uranium by cells and S-layer sheets of Bacillus sphaericus JG-A12. Appl Environ Microbiol 71:5532–5543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michalsen MM, Peacock AD, Spain AM, Smithgal AN, White DC, Sanchez-Rosario Y, Krumholz LR, Istok JD (2007) Changes in microbial community composition and geochemistry during uranium and technetium bioimmobilization. Appl Environ Microbiol 73:5885–5896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller CL, Landa ER, Updegraff DM (1987) Ecological aspects of microorganisms inhabiting uranium mill tailings. Microb Ecol 14:141–155

    Article  CAS  PubMed  Google Scholar 

  • Mondani L, Benzerara K, Carrière M, Christen R, Mamindy-Pajany Y, Février L, Marmier N, Achouak W, Nardoux P, Berthomieu C, Chapon V (2011) Influence of uranium on bacterial communities: a comparison of natural uranium-rich soils with controls. PLoS One 6:e25771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mosher JJ, Phelps TJ, Podar M, Hurt RA Jr, Campbell JH, Drake MM, Moberly JG, Schadt CW, Brown SD, Hazen TC, Arkin AP, Palumbo AV, Faybishenko BA, Elias DA (2012) Microbial community succession during lactate amendment and electron acceptor limitation reveals a predominance of metal-reducing Pelosinus spp. Appl Environ Microbiol 78:2082–2091

    Article  CAS  PubMed  PubMed Central  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  PubMed  Google Scholar 

  • Nilgiriwala KS, Alahari A, Rao AS, Apte SK (2008) Cloning and over expression of alkaline phosphatase PhoK from Sphingomonas sp. strain BSAR-1 for bioprecipitation of uranium from alkaline solutions. Appl Environ Microbiol 74:5516–5523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nostrand JDV, Wu L, Wu WM, Huang Z, Gentry TJ, Deng Y, Carley J, Carroll S, He Z, Gu B, Luo J, Criddle CS, Watson DB, Jardine PM, Marsh TL, Tiedje JM, Hazen TC, Zhou J (2011) Dynamics of microbial community composition and function during in situ bioremediation of a uranium contaminated aquifer. Appl Environ Microbiol 77:3860–3869

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • OECD (2008) Consensus document on information used in the assessment of environmental applications involving Acinetobacter, Series on harmonization of regulatory oversight in biotechnology No. 46. Organisation for Economic Co-operation and Development (OECD), Paris

    Google Scholar 

  • Panak P, Hard BC, Pietzsch K, Kutschke S, Röske K, Selenska-Pobell S, Bernhard G, Nitsche H (1998) Bacteria from uranium mining waste pile: interactions with U(VI). J Alloys Compd 271–273:1

    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 

  • Pereira SG, Albuquerque L, Nobre MF, Tiago I, Veríssimo A, Pereira A, da Costa MS (2012) Pullulanibacillus uraniitolerans sp. nov., a new acidophilic, U(VI)-resistant species isolated from an acid uranium mill tailing effluent and emended description of the genus Pullulanibacillus. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijs.0.040923-0

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pollmann K, Raff J, Merroun M, Fahmy K, Selenska-Pobell S (2005) Metal binding by bacteria from uranium mining waste piles and its technological applications. Biotechnol Adv 24:58–68

    Article  PubMed  CAS  Google Scholar 

  • Porat I, Vishnivetskaya TA, Mosher JJ, Brandt CC, Yang ZK, Brooks SC, Liang L, Drake MM, Podar M, Brown SD, Palumbo AV (2010) Characterization of archaeal community in contaminated and uncontaminated surface stream sediments. Microb Ecol 60:784–795

    Article  PubMed  PubMed Central  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 Microbiol 3:546–553

    Article  CAS  Google Scholar 

  • Radeva G, Selenska-Pobell S (2005) Bacterial diversity in water samples from uranium wastes as demonstrated by 16S rDNA and ribosomal intergenic spacer amplification retrievals. Can J Microbiol 51:910–923

    Article  CAS  PubMed  Google Scholar 

  • Radeva G, Kenarova A, Bachvarova V, Flemming K, Popov I, Vassilev D, Selenska-Pobell S (2013) Bacterial diversity at abandoned uranium mining and milling sites in Bulgaria as revealed by 16S rRNA genetic diversity study. Water Air Soil Pollut 224:1–14

    Article  CAS  Google Scholar 

  • Radeva G, Kenarova A, Bachvarova V, Flemming K, Popov I, Vassilev D, Selenska-Pobell S (2014) Phylogenetic diversity of archaea and the Archaeal ammonia Monooxygenase gene in uranium mining-impacted locations in Bulgaria. Archaea 2014:1–10

    Google Scholar 

  • Ragon M, Restoux G, Moreira D, Møller AP, López-García P (2011) Sunlight-exposed biofilm microbial communities are naturally resistant to chernobyl ionizing-radiation levels. PLoS One 6:e21764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rastogi G, Osman S, Kukkadapu R, Engelhard M, Vaishampayan P, Andersen G, Sani R (2010a) Microbial and mineralogical characterizations of soils collected from the deep biosphere of the former Homestake Gold Mine, South Dakota. Microb Ecol 60:539–550

    Article  CAS  PubMed  Google Scholar 

  • Rastogi G, Osman S, Vaishampayan P, Andersen G, Stetler L, Sani R (2010b) Microbial diversity in uranium mining-impacted soils as revealed by high-density 16S microarray and clone library. Microb Ecol 59:94–108

    Article  CAS  PubMed  Google Scholar 

  • Reardon CL, Cummings DE, Petzke LM, Kinsall BL, Watson DB, Peyton BM, Geesey GG (2004) Composition and diversity of microbial communities recovered from surrogate minerals incubated in an acidic uranium-contaminated aquifer. Appl Environ Microbiol 70:6037–6046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rittmann BE, Hausner M, Löffler F, Love NG, Muyzer G, Okabe S, Oerther DB, Peccia J, Raskin L, Wagner M (2006) A vista for microbial ecology and environmental biotechnology. Environ Sci Technol 40:1096–1103

    Article  PubMed  Google Scholar 

  • Sánchez-Castro I, Amador-García A, Moreno-Romero C, López-Fernández M, Phrommavanh V, Nos J, Descostes M, Merroun ML (2017) Screening of bacterial strains isolated from uranium mill tailings porewaters for bioremediation purposes. J Environ Radioact 166:130–141

    Google Scholar 

  • Satchanska G, Selenska-Pobell S (2005) Bacterial diversity in the uranium mill-tailings Gittersee as estimated via a 16S rDNA approach. C R Acad Bulg Sci 58:1105–1112

    CAS  Google Scholar 

  • Satchanska G, Golovinsky E, Selenska-Pobell S (2004) Bacterial diversity in a soil sample from uranium mining waste pile as estimated via a culture-independent 16S rDNA approach. C R Acad Bulg Sci 57:75–82

    CAS  Google Scholar 

  • Schippers A, Hallmann R, Wentzien S, Sand W (1995) Microbial diversity in uranium mine waste heaps. Appl Environ Microbiol 61:2930–2935

    CAS  PubMed  PubMed Central  Google Scholar 

  • Selenska-Pobell S (2002) Diversity and activity of bacteria in uranium waste piles. In: Keith-Roach M, Livens F (eds) Interactions of microorganisms with radionuclides. Elsevier, Oxford, pp 225–253

    Chapter  Google Scholar 

  • Selenska-Pobell S, Panak P, Miteva V, Boudakov I, Bernhard G, Nitsche H (1999) Selective accumulation of heavy metals by three indigenous 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 

  • Selenska-Pobell S, Kampf G, Hemming K, Radeva G, Satchanska G (2001) Bacterial diversity in soil samples from two uranium waste piles as determined by rep-APD, RISA and 16S rDNA retrieval. Anton Van Leeuw 79:149–161

    Article  CAS  Google Scholar 

  • Selenska-Pobell S, Flemming K, Tzvetkova T, Raff J, Schnorpfeil M, Geißler A (2002) Bacterial communities in uranium mining waste piles and their interaction with heavy metals. In: Merkel BJ, Planer-Friedrich B, Wolkersdorfer C (eds) Uranium in the aquatic environment. Springer, Berlin

    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  PubMed  PubMed Central  Google Scholar 

  • Silver M (1987) Distribution of iron-oxidizing bacteria in the nordic uranium tailings deposit, Elliot Lake, Ontario, Canada. Appl Environ Microbiol 53:846–852

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sitte J, Löffler S, Burkhardt EM, Goldfarb KC, Büchel G, Hazen TC, Küsel K (2015) Metals other than uranium affected microbial community composition in a historical uranium-mining site. Environ Sci Pollut Res 22:19326

    Article  CAS  Google Scholar 

  • Sivaswamy V, Boyanov MI, Peyton BM, Viamajala S, Gerlach R, Apel WA, Sani RK, Dohnalkova A, Kemner KM, Borch T (2011) Multiple mechanisms of uranium immobilization by Cellulomonas sp. strain ES6. Biotechnol Bioeng 108:264–276

    Article  CAS  PubMed  Google Scholar 

  • Stein LY, Jones G, Alexander B, Elmund K, Wright-Jones C, Nealson KH (2002) Intriguing microbial diversity associated with metal-rich particles from a freshwater reservoir. FEMS Microbiol Ecol 42:431–440

    Article  CAS  PubMed  Google Scholar 

  • Strandberg GW, Shumate SE, Parrott JR (1981) Microbial cells as biosorbents for heavy metals: accumulation of uranium by Saccharomyces cerevisiae and Pseudomonas aeruginosa. Appl Environ Microbiol 41:237–245

    CAS  PubMed  PubMed Central  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, DC, pp 393–432

    Google Scholar 

  • Suzuki SY, Banfield JF (2004) Resistance to, and accumulation of, uranium by bacteria from a uranium-contaminated. Geomicrobiol J 21:113–121

    Article  CAS  Google Scholar 

  • Suzuki SY, Suko T (2006) Geomicrobiological factors that control uranium mobility in the environment: Update on recent advances in the bioremediation of uranium-contaminated sites. J Mineral Petrol Sci 101:299–307

    Article  CAS  Google Scholar 

  • Suzuki Y, Kelly SD, Kemner KM, Banfield JF (2005) Direct microbial reduction and subsequent preservation of uranium in natural nearsurface sediment. Appl Environ Microbiol 71:1790–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tabak HH, Lens P, van Hullebusch ED, Dejonghe W (2005) 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. Rev Environ Sci Biotechnol 4:115–156

    Article  CAS  Google Scholar 

  • Takai K, Moser DP, DeFlaun M, Onstott TC, Fredrickson JK (2001) Archaeal diversity in waters from deep South African gold mines. Appl Environ Microbiol 67:5750–5760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  CAS  Google Scholar 

  • Tsezos M, Volesky B (1981) Biosorption of uranium and thorium. Biotechnol Bioeng 23:583–604

    Article  CAS  Google Scholar 

  • Tsezos M, Remoudaki E, Angelatou V (1997) Biosorption sites of selected metals using electron microscopy. Comp Biochem Physiol 118A:481–487

    Article  CAS  Google Scholar 

  • Tsuruta T (2007) Removal and recovery of uranium using microorganisms isolated from North American uranium deposits. Am J EnvironSci 3:60–66

    CAS  Google Scholar 

  • Waldron PJ, Wu L, Van Nostrand JD, Schadt CW, He Z, Watson DB, Jardine PM, Palumbo AV, Hazen TC, Zhou J (2009) Functional gene array-based analysis of microbial community structure in groundwaters with a gradient of contaminant levels. Environ Sci Technol 43:3529–3534

    Article  CAS  PubMed  Google Scholar 

  • Wolfaardt GM, Hendry MJ, Korber DR (2008) Microbial distribution and diversity in saturated, high pH, uranium mine tailings, Saskatchewan, Canada. Can J Microbiol 54:932–940

    Article  CAS  PubMed  Google Scholar 

  • 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 B, Watson D, Cirpka OA, Zhou J, 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  CAS  PubMed  Google Scholar 

  • Yan X, Luo X (2015) Radionuclides distribution, properties, and microbial diversity of soils in uranium mill tailings from southeastern China. J Environ Radioact 139:85–90

    Google Scholar 

  • Yi Z, Lian B (2012) Adsorption of U(VI) by Bacillus mucilaginosus. J Radioanal Nucl Chem 293:321–329

    Article  CAS  Google Scholar 

  • Yong P, Macaskie LE (1998) Bioaccumulation of lanthanum, uranium and thorium, and use of a model system to develop a method for the biologically-mediated removal of plutonium from solution. J Chem Technol Biotechnol 71:15–26

    Article  CAS  Google Scholar 

  • Zhang P, Wu W-M, Van Nostrand J, Deng Y, He Z, Gihring T et al (2015) Dynamic succession of groundwater functional microbial communities in response to emulsified vegetable oil amendment during sustained in situ U(VI) reduction. Appl Environ Microbiol 81:4164–4172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan X, Luo X, Zhao M (2016) Metagenomic analysis of microbial community in uranium-contaminated soil. Appl Microbiol Biotechnol 100(1):299–310

    Google Scholar 

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Dhal, P.K. (2018). Bacterial Communities of Uranium-Contaminated Tailing Ponds and Their Interactions with Different Heavy Metals. In: Adhya, T., Lal, B., Mohapatra, B., Paul, D., Das, S. (eds) Advances in Soil Microbiology: Recent Trends and Future Prospects. Microorganisms for Sustainability, vol 3. Springer, Singapore. https://doi.org/10.1007/978-981-10-6178-3_6

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