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Emerging Environmental Technologies, Volume II pp 1–37Cite as

Immobilization of Uranium in Groundwater Using Biofilms

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Abstract

Uranium is one of the most common radionuclides in soils, sediments, and groundwater at radionuclides-contaminated sites. At these contaminated sites, uranium leaches into the groundwater, which has become a widespread problem at mining and milling sites across North America, South America, and Eastern Europe. The movement of groundwater usually transports soluble uranium contaminants beyond their original boundaries, causing a global problem in aquifers, water supplies, and related ecosystems and posing a serious threat to human health and the natural environment. In order to meet the EPA standards, extensive efforts have been made to assess and remediate uranium-contaminated sites. As a cost-effective technology with minimal disruption to the environment, bioremediation harnessing indigenous microbial processes for cleanup has been utilized for uranium remediation. In the first part of this chapter, various uranium remediation technologies are discussed. Emphasis is placed on the principles and mechanisms of uranium bioremediation and the key factors affecting it. The second part of this chapter focuses on the use of biofilms for uranium immobilization in groundwater from subsurface environments. Most of the literature studies on uranium bioremediation have been conducted with suspended microorganisms or enriched sediments, which were eventually spiked with micro- or nano-particles of other minerals. However, biofilms are the commonly found microbial growth pattern in natural soils and water-sediment interfaces. With heterogeneous and complex biotic, abiotic and redox conditions significantly different from those in bulk conditions, biofilms pose challenges in predicting the mobility of uranium. Although previous studies have improved our understanding of uranium immobilization processes in biofilms, in order to efficiently and sustainably immobilize uranium at contaminated sites using indigenous biofilms, more knowledge is needed on the complex interactions among uranium, biofilms, and various redox-sensitive minerals during in situ uranium bioremediation.

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Abbreviations

DU:

Depleted Uranium

EPA:

Environmental Protection Agency

MCL:

Maximum Contaminant Level

PRBs:

Permeable Reactive Barriers

DMRB:

Dissimilatory Metal-Reducing Bacteria

LPS:

Lipopolysaccharide

EPS:

Extracellular Polymeric Substances

UMTRA:

Uranium Mill Tailing Remedial Action

Eh :

Electrochemical Potential

VSHE :

Potential Against Standard Hydrogen Electrode Potential

DIRB:

Dissimilatory Iron-Reducing Bacteria

SRB:

Sulfate-Reducing Bacteria

FBCR:

Fixed Bed Column Reactor

TEM:

Transmission Electron Microscopy

SAED:

Selected Area Electron Diffraction

EDS:

Energy-Dispersive Spectrometry

HRTEM:

High-Resolution Transmission Electron Microscopy

References

  1. Fan, A., and G. Alexeeff. 2001. Public Health Goal for Uranium in Drinking Water. Office of Environmental Health Hazard Assessment, California Environmental Protection Agency, Oakland, CA.

    Google Scholar 

  2. NRC. 1983. Uranium, Vol. 5. National Research Council, Washington, DC.

    Google Scholar 

  3. Merroun, M., and S. Selenska-Pobell. 2008. Bacterial interactions with uranium: an environmental perspective. Journal of Contaminant Hydrology 102: 285–295.

    Article  CAS  Google Scholar 

  4. N‘Guessan, A., H. Varionis, C. Resch, P. Long, and D. Lovley. 2008. Sustained removal of uranium from contaminated groundwater following stimulation of dissimilatory metal reduction. Environmental Science and Technology 42: 2999–3004.

    Article  CAS  Google Scholar 

  5. Abdelouas, A., W. Lutze, and H. Nuttall. 1999. Uranium contamination in the subsurface: characterization and remediation. Reviews in Mineralogy and Geochemistry 38: 433–473.

    CAS  Google Scholar 

  6. Akob, D., H. Mills, T. Gihring, L. Kerkhof, J. Stucki, A. Anastacio, K. Chin, K. Kusel, A. Palumbo, D. Watson, and J. Kostka. 2008. Functional diversity and electron donor dependence of microbial populations capable of U(VI) reduction in radionuclide-contaminated subsurface sediments. Applied and Environmental Microbiology 74: 3159–3170.

    Article  CAS  Google Scholar 

  7. Sani, R., B. Peyton, and A. Dohnalkova. 2008. Comparison of uranium(VI) removal by Shewanella oneidensis MR-1 in flow and batch reactors. Water Research 42: 2993–3002.

    Article  CAS  Google Scholar 

  8. Vrionis, H., R. Anderson, I. Ortiz-Bernad, K. O‘Neill, C. Resch, A. Peacock, R. Dayvault, D. White, P. Long, and D. Lovley. 2005. Microbiological and geochemical heterogeneity in an in situ uranium bioremediation field site. Applied and Environmental Microbiology 71: 6308–6318.

    Article  CAS  Google Scholar 

  9. Zhu, G., X. Xiang, X. Chen, L. Wang, H. Hu, and S. Weng. 2008. Renal dysfunction induced by long-term exposure to depleted uranium in rats. Archives of Toxicology 83: 37–46.

    Article  CAS  Google Scholar 

  10. Bleise, A., P. Danesi, and W. Burkart. 2003. Properties, use and health effects of depleted uranium (DU): a general overview. Journal of Environmental Radioactivity 64: 93–112.

    Article  CAS  Google Scholar 

  11. Landa, E., and J. Gray. 1995. Us geological survey- research on the environmental fate of uranium mining and milling wastes. Environmental Geology 26: 19–31.

    Article  CAS  Google Scholar 

  12. Suzuki, Y., and T. Suko. 2006. Geomicrobiological factors that control uranium mobility in the environment: update on recent advances in the bioremediation of uranium-contaminated sites. Journal of Mineralogical and Petrological Sciences 101: 299–307.

    Article  CAS  Google Scholar 

  13. McClain, D., A. Miller, and J. Kalinich. 2005. Presented at the Radiation Bioeffects and Countermeasures, Bethesda, Maryland, USA.

    Google Scholar 

  14. Todorov, P., and E. Ilieva. 2006. Contamination with uranium from natural and antropological sources. Romanian Journal of Physics 51: 27–34.

    CAS  Google Scholar 

  15. EPA. 2002. EPA Facts About Uranium. U. S. E. P. Agency, Washington, DC.

    Google Scholar 

  16. Milacic, S.. 2008. Health investigations of depleted uranium clean-up workers. Medicina del Lavoro 99: 366–370.

    CAS  Google Scholar 

  17. EPA. 2006. Drinking Water Standards and Health Advisories. U. S. E. P. Agency, Washington, DC.

    Google Scholar 

  18. Beyenal, H., R. Sani, B. Peyton, A. Dohnalkova, J. Amonette, and Z. Lewandowski. 2004. Uranium immobilization by sulfate-reducing biofilms. Environmental Science and Technology 38: 2067–2074.

    Article  CAS  Google Scholar 

  19. 19. Hu, Q., J. Weng, and J. Wang. 2009. Sources of anthropogenic radionuclides in the environment: a review. Journal of Environmental Radioactivity DOI 10.1016/j.jenvrad.2008.08.004.

    Google Scholar 

  20. EPA 2001, Posting date. A citizen’s guide to pump and treat. http://www.clu-in.org/download/citizens/pump_and_treat.pdf. [Online.]

  21. Fuller, C., J. Bargar, J. Davis, and M. Piana. 2002. Mechanisms of uranium interactions with hydroxyapatite: implications for groundwater remediation. Environmental Science and Technology 36: 158–165.

    Article  CAS  Google Scholar 

  22. Morrison, S., D. Metzler, and C. Carpenter. 2001. Uranium precipitation in a permeable reactive barrier by progressive irreversible dissolution of zerovalent iron. Environmental Science and Technology 35: 385–390.

    Article  CAS  Google Scholar 

  23. Morrison, S., P. Mushovic, and P. Niesen. 2006. Early breakthrough of molybdenum and uranium in a permeable reactive barrier. Environmental Science and Technology 40: 2018–2024.

    Article  CAS  Google Scholar 

  24. Simon, F., V. Biermann, and B. Peplinski. 2008. Uranium removal from groundwater using hydroxyapatite. Applied Geochemistry 23: 2137–2145.

    Article  CAS  Google Scholar 

  25. Martinez, R.. 2008. Multiscale Analyses of Microbial Populations in Extreme Environments. PhD Dissertation. Georgia Institute of Technology, Atlanta, Georgia.

    Google Scholar 

  26. Hwang, C., W. Wu, T. Gentry, J. Carley, G. Corbin, S. Carroll, D. Watson, P. Jardine, J. Zhou, C. Criddle, and M. Fields. 2009. Bacterial community succession during in situ uranium bioremediation: spatial similarities along controlled flow paths. ISME Journal 3: 47–64.

    Article  CAS  Google Scholar 

  27. Wall, J., and L. Krumholz. 2006. Uranium reduction. Annual Reviews of Microbiology 60: 149–166.

    Article  CAS  Google Scholar 

  28. Philip, J., S. Bamforth, I. Singleton, and R. Atlas. 2005. Environmental Pollution and Restoration: A Role for Bioremediation. ASM Press, Washington, DC.

    Google Scholar 

  29. Watanabe, M.. 2001. Can bioremediation bounce back?. Nature Biotechnology 19: 1111–1115.

    Article  CAS  Google Scholar 

  30. NABIR. 2003. Bioremediation of metals and radionuclides: what it is and how it works. LBNL–42595.

    Google Scholar 

  31. Gadd, G.. 2001. Microbial metal transformations. Journal of Microbiology 39: 83–88.

    CAS  Google Scholar 

  32. Hazen, T., and H. Tabak. 2005. Developments in bioremediation of soils and sediments polluted with metals and radionuclides: 2. Field research on bioremediation of metals and radionuclides. Reviews in Environmental Science and Bio/Technology 4: 157–183.

    Article  CAS  Google Scholar 

  33. Gorby, Y., and D. Lovley. 1992. Enzymatic uranium precipitation. Environmental Science and Technology 26: 205–207.

    Article  CAS  Google Scholar 

  34. Lovley, D., E. Phillips, Y. Gorby, and E. Landa. 1991. Microbial reduction of uranium. Nature 350: 413–416.

    Article  CAS  Google Scholar 

  35. Kumar, R., S. Singh, and O. Singh. 2007. Bioremediation of radionuclides: emerging technologies. OMICS A Journal of Integrative Biology 11: 295–304.

    Article  CAS  Google Scholar 

  36. Woolfolk, C., and H. Whiteley. 1962. Reduction of inorganic compounds with molecular hydrogen by Micrococcus lactilyticus. I. Stoichiometry with compounds of arsenic, selenium, tellurium, transitions and other elements. Journal of Bacteriology 84: 647–658.

    CAS  Google Scholar 

  37. Lovley, D., and E. Phillips. 1992. Reduction of uranium by Desulfovibrio desulfuricans. Applied and Environmental Microbiology 58: 850–856.

    CAS  Google Scholar 

  38. Renshaw, J., L. Butchins, F. Livens, I. May, J. Charnock, and J. Lloyd. 2005. Bioreduction of uranium: environmental implications of a pentavalent intermediate. Environmental Science and Technology 39: 5657–5660.

    Article  CAS  Google Scholar 

  39. McLean, J., and T. Beveridge. 2001. Chromate reduction by a pseudomonad isolated from a site contaminated with chromated copper arsenate. Applied and Environmental Microbiology 67: 1076–1084.

    Article  CAS  Google Scholar 

  40. Sani, R., B. Peyton, and A. Dohnalkova. 2004. Presented at the ASM 104th General Meeting.

    Google Scholar 

  41. Liu, C., Y. Gorby, J. Zachara, J. Fredrickson, and C. Brown. 2002. Reduction kinetics of Fe(III), Co(III), U(VI), Cr(VI), Tc(VII) in cultures of dissimilatory metal-reducing bacteria. Biotechnology and Bioengineering 80: 637–649.

    Article  CAS  Google Scholar 

  42. Lloyd, J., C. Leang, A. Hodges-Myerson, M. Coppi, S. Cuifo, B. Methe, S. Sandler, and D. Lovley. 2003. Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochemical Journal 369: 153–161.

    Article  CAS  Google Scholar 

  43. Suzuki, Y., S. Kelly, K. Kemner, and J. Banfield. 2004. Enzymatic U(VI) reduction by Desulfosporosinus species. Radiochimica Acta 92: 11–16.

    Article  CAS  Google Scholar 

  44. Renshaw, J., J. Lloyd, and F. Livens. 2007. Microbial interactions with actinides and long-lived fission products. Comptes Rendus Chimie 10: 1067–1077.

    Article  CAS  Google Scholar 

  45. Akhtar, K., M. Akhtar, and A. Khalid. 2007. Removal and recovery of uranium from aqueous solutions by Trichoderma harzianum. Water Research 41: 1366–1378.

    Article  CAS  Google Scholar 

  46. Choi, J., J. Lee, and J. Yang. 2009. Biosorption of heavy metals and uranium by starfish and Pseudomonas putida. Journal of Hazardous Materials 161: 157–162.

    Article  CAS  Google Scholar 

  47. Kalin, M., W. Wheeler, and G. Meinrath. 2004. The removal of uranium from mining waste water using algal/microbial biomass. Journal of Environmental Radioactivity 78: 151–177.

    Article  CAS  Google Scholar 

  48. Ohnuki, T., T. Yoshida, T. Ozaki, M. Samadfam, N. Kozai, K. Yubuta, T. Mitsugashira, T. Kasama, and A. Francis. 2005. Interactions of uranium with bacteria and kaolinite clay. Chemical Geology 220: 237–243.

    Article  CAS  Google Scholar 

  49. Wang, J., and C. Chen. 2006. Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnology Advances 24: 427–451.

    Article  CAS  Google Scholar 

  50. Beazley, M., R. Martinez, P. Sobecky, S. Webb, and M. Taillefert. 2007. Uranium biomineralization as a result of bacterial phosphatase activity: insight from bacterial isolates from a contaminated subsurface. Environmental Science and Technology 41: 5701–5707.

    Article  CAS  Google Scholar 

  51. Martinez, R., M. Beazley, M. Taillefert, A. Arakaki, J. Skolnick, and P. Sobecky. 2007. Aerobic uranium (VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide- and metal-contaminated subsurface soils. Environmental Microbiology 9: 3122–3133.

    Article  CAS  Google Scholar 

  52. Renninger, N., R. Knopp, H. Nitsche, D. Clark, and J. Keasling. 2004. Uranyl precipitation by Pseudomonas aeruginosa via controlled polyphosphate metabolism. Applied and Environmental Microbiology 70: 7404–7412.

    Article  CAS  Google Scholar 

  53. Rodriguez-Navarro, C., M. Rodriguez-Gallego, K. Benchekroun, and M. Gonzalez-Munoz. 2003. Conservation of ornamental stone by Myxococcus xanthus-induced carbonate biomineralization. Applied and Environmental Microbiology 69: 2182–2193.

    Article  CAS  Google Scholar 

  54. Vazquez, G., C. Dodge, and A. Francis. 2007. Interactions of uranium with polyphosphate. Chemosphere 70: 263–269.

    Article  CAS  Google Scholar 

  55. Merroun, M., M. Nedelkova, A. Rossberg, C. Hennig, and S. Selenska-Pobell. 2006. Interaction mechanisms of uranium with bacterial strains isolated from extreme habitats. Radiochimica Acta 94: 723–729.

    Article  CAS  Google Scholar 

  56. Suzuki, Y., and J. Banfield. 1999. Uranium: Mineralogy, Geochemistry and the Environment. Mineralogical Society of America, Chantilly, VA .

    Google Scholar 

  57. Abdelouas, A., Y. Lu, W. Lutze, and H. Nuttall. 1998. Reduction of U(VI) to U(IV) by indigenous bacteria in contaminated ground water. Journal of Contaminant Hydrology 35: 217–233.

    Article  CAS  Google Scholar 

  58. Elias, D., L. Krumholz, D. Wong, P. Long, and J. Suflita. 2003. Characterization of microbial activities and U reduction in a shallow aquifer contaminated by uranium mill tailings. Microbial Ecology 46: 83–91.

    Article  CAS  Google Scholar 

  59. Senko, J., J. Istok, J. Suflita, and L. Krumholz. 2002. In-situ evidence for uranium immobilization and remobilization. Environmental Science and Technology 36: 1491–1496.

    Article  CAS  Google Scholar 

  60. Gu, B., W. Wu, M. Ginder-Vogel, H. Yan, M. Fields, J. Zhou, S. Fendorf, C. Criddle, and P. Jardine. 2005. Bioreduction of uranium in a contaminated soil column. Environmental Science and Technology 39: 4841–4847.

    Article  CAS  Google Scholar 

  61. Ortiz-Bernad, I., R. Anderson, H. Vrionis, and D. Lovley. 2004. Resistance of solid-phase U(VI) to microbial reduction during in situ bioremediation of uranium-contaminated groundwater. Applied and Environmental Microbiology 70: 7558–7560.

    Article  CAS  Google Scholar 

  62. Langmuir, D.. 1978. Uranium solution-mineral equilibria at low temperatures with applications to sedimentary ore deposits. Geochimica et Cosmochimica Acta 42: 547–569.

    Article  CAS  Google Scholar 

  63. Brooks, S., J. Fredrickson, S. Carroll, D. Kennedy, J. Zachara, A. Plymale, S. Kelly, K. Kemner, and S. Fendorf. 2003. Inhibition of bacterial U(VI) reduction by calcium. Environmental Science and Technology 37: 1850–1858.

    Article  CAS  Google Scholar 

  64. Lloyd, J., and L. Macaskie. 2000. Bioremediation of Raionuclide-Contaminated Wastewaters. ASM Press, Washington, DC.

    Google Scholar 

  65. Fredrickson, J., J. Zachara, D. Kennedy, C. Liu, M. Duff, D. Hunter, and A. Dohnalkova. 2002. Influence of Mn oxides on the reduction of uranium(VI) by metal-reducing bacterium Shewanella putrefaciens. Geochimica et Cosmochimica Acta 66: 3247–3262.

    Article  CAS  Google Scholar 

  66. Moon, H., J. Komlos, and P. Jaffe. 2009. Biogenic U(IV) oxidation by dissolved oxygen and nitrate in sediment after prolonged U(VI)/Fe(III)/SO42- reduction. Journal of Contaminant Hydrology 105: 18–27.

    Article  CAS  Google Scholar 

  67. Sani, R., B. Peyton, J. Amonette, and G. Geesey. 2004. Reduction of uranium(VI) under sulfate-reducing conditions in the presence of Fe(III)-(hydr)oxides. Geochimica et Cosmochimica Acta 68: 2639–2648.

    Article  CAS  Google Scholar 

  68. Finch, R., and T. Murakami. 1999. Systematics and paragenesis of uranium minerals. Reviews in Mineralogy 38: 91–179.

    CAS  Google Scholar 

  69. Fredrickson, J., J. Zachara, D. Kennedy, M. Duff, Y. Gorby, S. Li, and K. Krupka. 2000. Reduction of U(VI) in goethite (alpha-FeOOH) suspensions by a disimilatory metal-reducing bacterium. Geochimica et Cosmochimica Acta 64: 3085–3098.

    Article  CAS  Google Scholar 

  70. Anderson, R.. 1987. Redox behavior of uranium in an anoxic marine basin. Uranium 3: 145–164.

    CAS  Google Scholar 

  71. Marshall, M., A. Beliaev, A. Dohnalkova, D. Kennedy, L. Shi, Z. Wang, M. Boyanov, B. Lai, K. Kemner, J. McLean, S. Reed, D. Culley, V. Bailey, C. Simonson, D. Saffarini, M. Romine, J. Zachara, and J. Fredrickson. 2006. c-Type cytochrome-dependent formation of U(IV) nanoparticles by Shewanella oneidensis. PLoS Biology 4: 1324–1333.

    Article  CAS  Google Scholar 

  72. Marshall, M., A. Dohnalkova, D. Kennedy, A. Plymale, S. Thomas, F. Loffler, R. Sanford, J. Zachara, J. Fredrickson, and A. Beliaev. 2009. Electron donor-dependent radionuclide reduction and nanoparticle formation by Anaeromyxobacter dehalogenans strain 2CP-C. Environmental Microbiology 11: 534–543.

    Article  CAS  Google Scholar 

  73. Marsili, E., H. Beyenal, L. Palma, C. Merli, A. Dohnalkova, J. Amonette, and Z. Lewandowski. 2005. Uranium removal by sulfate reducing biofilms in the presence of carbonates. Water Science and Technology 52: 49–55.

    CAS  Google Scholar 

  74. Suzuki, Y., S. Kelly, K. Kemner, and J. Banfield. 2005. Direct microbial reduction and subsequent preservation of uranium in natural near-surface sediment. Applied and Environmental Microbiology 71: 1790–1797.

    Article  CAS  Google Scholar 

  75. Francis, A., and C. Dodge. 2008. Bioreduction of uranium(VI) complexed with citric acid by Clostridia affects its structure and solubility. Environmental Science and Technology 42: 8277–8282.

    Article  CAS  Google Scholar 

  76. Lovley, D., and E. Phillips. 1992. Bioremediation of uranium contamination with enzymatic uranium reduction. Environmental Science and Technology 26: 2228–2234.

    Article  CAS  Google Scholar 

  77. Lovley, D., E. Roden, E. Phillips, and J. Woodhard. 1993. Enzymatic iron and uranium reduction by sulfate-reducing bacteria. Marine Geology 113: 41–53.

    Article  CAS  Google Scholar 

  78. Yi, Z., K. Tan, A. Tan, Z. Yu, and S. Wang. 2007. Influence of environmental factors on reductive bioprecipitation of uranium by sulfate reducing bacteria. International of Biodeterioration & Biodegradation 60: 258–266.

    Article  CAS  Google Scholar 

  79. Cooke, A., R. Rowe, B. Rittman, and I. Flemming. 1999. Modelling biochemically driven mineral precipitation in anaerobic biofilms. Water Science and Technology 39: 57–64.

    Article  CAS  Google Scholar 

  80. Decho, A.. 2000. Microbial biofilms in intertidal systems: an overview. Continental Shelf Research 20: 1257–1273.

    Article  Google Scholar 

  81. Nelson, Y., L. Lion, M. Shuler, and W. Ghiorse. 1999. Lead binding to metal oxide and organic phases of natural aquatic biofilms. Limnology and Oceanography 44: 1715–1729.

    Article  CAS  Google Scholar 

  82. Beyenal, H., and Z. Lewandowski. 2004. Dynamics of lead immobilization in sulfate reducing biofilms. Water Research 38: 2726–2736.

    Article  CAS  Google Scholar 

  83. Lewandowski, Z., and H. Beyenal. 2007. Fundamentals of Biofilm Research. CRC Press, Boca Rotan FL.

    Google Scholar 

  84. Edwards, L., K. Kusel, H. Drake, and J. Kostka. 2007. Electron flow in acidic subsurface sediments co-contaminated with nitrate and uranium. Geochimica et Cosmochimica Acta 71: 643–654.

    Article  CAS  Google Scholar 

  85. Finneran, K., M. Housewright, and D. Lovley. 2002. Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environmental Microbiology 4: 510–516.

    Article  CAS  Google Scholar 

  86. Peacock, A., Y. Chang, J. Istok, L. Krumholz, R. Geyer, B. Kinsall, D. Watson, K. Sublette, and D. White. 2004. Utilization of microbial biofilms as monitors of bioremediation. Microbial Ecology 47: 284–292.

    Article  CAS  Google Scholar 

  87. Marsili, E., H. Beyenal, L. Palma, C. Merli, A. Dohnalkova, J. Amonette, and Z. Lewandowski. 2007. Uranium immobilization by sulfate-reducing biofilms grown on hematite, dolomite, and calcite. Environmental Science and Technology 41: 8349–8354.

    Article  CAS  Google Scholar 

  88. Muyzer, G., and A. Stams. 2008. The ecology and biotechnology of sulphate-reducing bacteria. Nature Reviews Microbiology 6: 441–454.

    CAS  Google Scholar 

  89. van Hullebusch, E., M. Zandvoort, and P. Lens. 2003. Metal immobilization by biofilms: mechanisms and analytical tools. Reviews in Environmental Science and Bio/Technology 2: 9–33.

    Article  Google Scholar 

  90. Sarro, M., A. Garcia, and D. Moreno. 2005. Biofilm formation in spent nuclear fuel pools and bioremediation of radioactive water. International Microbiology 8: 223–230.

    CAS  Google Scholar 

  91. Mohagheghi, A., D. Updegraff, and M. Goldhaber. 1985. The role of sulfate-reducing bacteria in the deposition of sedimentary uranium ores. Geomicrobiology Journal 4: 153–173.

    Article  CAS  Google Scholar 

  92. Spear, J., L. Figueroa, and B. Honeyman. 1999. Modeling the Removal of Uranium U(VI) from Aqueous Solutions in the Presence of Sulfate Reducing Bacteria. Environmental Science and Technology 33: 2667–2675.

    Article  CAS  Google Scholar 

  93. Hau, H. H., and J. A. Gralnick. 2007. Ecology and biotechnology of the genus Shewanella. Annual Reviews of Microbiology 61: 237–258.

    Article  CAS  Google Scholar 

  94. Majors, P., J. McLean, G. Pinchuk, J. Fredrickson, Y. Gorby, K. Minard, and R. Wind. 2005. NMR methods for in situ biofilm metabolism studies. Journal of Microbiological Methods 62: 337–344.

    Article  CAS  Google Scholar 

  95. McLean, J., P. Majors, C. Reardon, C. Bilskis, S. Reed, M. Romine, and J. Fredrickson. 2008. Investigation of structure and metabolism within Shewanella oneidensis MR-1 biofilms. Journal of Microbiological Methods 74: 47–56.

    Article  CAS  Google Scholar 

  96. Teal, T., D. Lies, B. Wold, and D. Newman. 2006. Spatiometabolic stratification of Shewanella oneidensis biofilms. Applied and Environmental Microbiology 72: 7324–7330.

    Article  CAS  Google Scholar 

  97. Ross, D., S. S. Ruebush, S. Brantley, R. Hartshorne, T. Clarke, D. Richardson, and M. Tien. 2007. Characterization of protein-protein interactions involved in iron redcution by Shewanella oneidensis MR-1. Applied and Environmental Microbiology 73: 5797–5808.

    Article  CAS  Google Scholar 

  98. Shi, L., T. Squier, J. Zachara, and J. Fredrickson. 2007. Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Molecular Microbiology 65: 12–20.

    Article  CAS  Google Scholar 

  99. Schwalb, C., S. Chapman, and G. Reid. 2002. The membrane-bound tetrahaem c-type cytochrome CymA interacts directly with the soluble fumarate reducatase in Shewanella. Biochemical Society Transactions 30: 658–662.

    Article  CAS  Google Scholar 

  100. Beliaev, A., D. Saffarini, J. McLaughlin, and D. Hunnicutt. 2001. MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Molecular Microbiology 39: 722–730.

    Article  CAS  Google Scholar 

  101. Gorby, Y., S. Yanina, J. McLean, K. Rosso, D. Moyles, A. Dohnalkova, T. Beveridge, I. Chang, B. Kim, K. Kim, D. Culley, S. Reed, M. Romine, D. Saffarini, E. Hill, L. Shi, D. Elias, D. Kennedy, G. Pinchuk, K. Watanabe, S. Ishii, B. Logan, K. Nealson, and J. Fredrickson. 2006. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. PNAS 103: 11358–11363.

    Article  CAS  Google Scholar 

  102. Lies, D., M. Hernandez, A. Kappler, R. Mielke, J. Gralnick, and D. Newman. 2005. Shewanella oneidensis MR-1 uses overlapping pathways for iron reduction at a distance and by direct contact under conditions relevant for biofilms. Applied and Environmental Microbiology 71: 4414–4426.

    Article  CAS  Google Scholar 

  103. Van der Zee, F., and F. Cervantes. 2009. Impact and application of electron shuttles on the redox (bio)transformation of contaminants: a review. Biotechnology Advances 27: 256–277.

    Article  CAS  Google Scholar 

  104. Hernandez, M., A. Kappler, and D. Newman. 2004. Phenazines and other redox-active antibiotics promote microbial mineral reduction. Applied and Environmental Microbiology 70: 921–928.

    Article  CAS  Google Scholar 

  105. Gu, B., H. Yan, P. Zhou, and D. Watson. 2005. Natural humics impact uranium bioreduction and oxidation. Environmental Science and Technology 39: 5268–5275.

    Article  CAS  Google Scholar 

  106. Marsili, E., D. B. Baron, I. D. Shikhare, D. Coursolle, J. A. Gralnick, and D. R. Bond. 2008. Shewanella secretes flavins that mediate extracellular electron transfer. Proceedings of the National Academy of Sciences of the United States of America 105: 3968–3973.

    Article  CAS  Google Scholar 

  107. von Canstein, H., J. Ogawa, S. Shimizu, and J. Lloyd. 2008. Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Applied and Environmental Microbiology 74: 615–623.

    Article  CAS  Google Scholar 

  108. Komlos, J., A. Peacock, R. Kukkadapu, and P. Jaffe. 2008. Long-term dynaimics of uranium reduction/reoxidation under low sulfate conditions. Geochimica et Cosmochimica Acta 72: 3603–3615.

    Article  CAS  Google Scholar 

  109. Moreels, D., G. Crosson, C. Garafola, D. Monteleone, S. Taghavi, J. Fitts, and D. van der Lelie. 2008. Microbial community dynamics in uranium contaminated subsurface sediments under biostimulated conditions with high nitrate and nickel pressure. Environmental Science and Pollution Reserach 15: 481–491.

    Article  CAS  Google Scholar 

  110. Boonchayaanant, B., B. Gu, M. Ortiz, and C. Criddle. 2009. Can microbially-generated hydrogen sulfide account for the trates of U(VI) reduction by a sulfate-reducing bacteria, DOE-ERSP 4th Annual PI Meeting 2009, Lansdowne, Virginia.

    Google Scholar 

  111. Joen, O., S. Kelly, K. Kemner, M. Barnett, W. Burgos, B. Dempsey, and E. Roden. 2004. Microbial reduction of U(VI) at the solid-water interface. Environmental Science and Technology 38: 5649–5655.

    Article  CAS  Google Scholar 

  112. Sanford, R., Q. Wu, Y. Sung, S. Thomas, B. Amos, E. Prince, and F. Loffler. 2007. Hexavalent uranium supports growth of Anaeromyxobacter dehalogenans and Geobacter spp. with lower than predicted biomass yields. Environmental Microbiology 9: 2885–2893.

    Article  CAS  Google Scholar 

  113. Wu, Q., R. Sanford, and F. Loffler. 2006. Uranium(VI) reduction by Anaeromyxobacter dehalogenans strain 2CP-C. Applied and Environmental Microbiology 72: 3608–3614.

    Article  CAS  Google Scholar 

  114. Sani, R., B. Peyton, W. Smith, W. Apel, and J. Petersen. 2002. Dissimilatory reduction of Cr(VI), Fe(III), and U(VI) by Cellulomonas isolates. Applied Microbiology and Biotechnology 60: 192–199.

    Article  CAS  Google Scholar 

  115. Francis, A., C. Dodge, F. Lu, G. Halada, and C. Clayton. 1994. XPS and XANES studies of uranium reduction by Clostridium sp.. Environmental Science and Technology 28: 636–639.

    Article  CAS  Google Scholar 

  116. Francis, A., G. Joshi-Tope, C. Dodge, and J. Gillow. 2002. Biotransformation of uranium and transition metal citrate complexes by Clostridia. Journal of Nuclear Science and Technology 3: 935–938.

    Google Scholar 

  117. Gao, W., and A. Francis. 2008. Reduction of uranium(VI) to uranium(IV) by Clostridia. Applied and Environmental Microbiology 74: 4580–4584.

    Article  CAS  Google Scholar 

  118. Appukuttan, D., A. Rao, and S. Apte. 2006. Engineering of Deinococcus radiodurans R1 for bioprecipitation of uranium from dilute nuclear waste. Applied and Environmental Microbiology 72: 7873–7878.

    Article  CAS  Google Scholar 

  119. Fredrickson, J., H. Kostandarithes, S. Li, A. Plymale, and M. Daly. 2000. Reduction of Fe(III), Cr(VI), U(VI), and Tc(VII) by Deinococcus radiodurans R1. Applied and Environmental Microbiology 66: 2006–2011.

    Article  CAS  Google Scholar 

  120. Tebo, B., and A. Obraztsova. 1998. Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and FE(III) as electron acceptors. FEMS Microbiology Letters 162: 193–198.

    Article  CAS  Google Scholar 

  121. Senko, J., G. Zhang, J. McDonough, M. Bruns, and W. Burgos. 2009. Metal reduction at low pH by a Desulfosporosinus species: implications for the biological treatment of acidic mine drainage. Geomicrobiology Journal 26: 71–82.

    Article  CAS  Google Scholar 

  122. Lovley, D., E. Roden, E. Phillips, and J. Woodward. 1993. Enzyamtic iron and uranium reduction by sulfate-reducing bacteria. Marine Geology 113: 41–53.

    Article  CAS  Google Scholar 

  123. Boonchayaanant, B., P. Kitanidis, and C. Criddle. 2008. Growth and cometabolic reduction kinetics of a uranium- and sulfate- reducing Desulfovibrio/Clostridia mixed culture: temperature effects. Biotechnology and Bioengineering 99: 1107–1119.

    Article  CAS  Google Scholar 

  124. Pietzsch, K., and W. Babel. 2003. A sulfate-reducing bacterium that can detoxify U(VI) and obtain energy via nitrate reduction. Journal of Basic Microbiology 43: 348–361.

    Article  CAS  Google Scholar 

  125. Pietzsch, K., B. Hard, and W. Babel. 1999. A Desulfovibrio sp. capable of growing by reducing U(VI). Journal of Basic Microbiology 39: 365–372.

    Article  CAS  Google Scholar 

  126. Payne, R., D. Gentry, B. Rapp-Giles, L. Casalot, and J. Wall. 2002. Uranium reduction by Desulfovibrio desulfuricans strain G20 and a cytochrome c3 mutant. Applied and Environmental Microbiology 68: 3129–3132.

    Article  CAS  Google Scholar 

  127. Kashefi, K., and D. Lovley. 2000. Reduction of Fe(III), Mn(IV), and Toxic Metals at 100°C by Pyrobaculum islandicum. Applied and Environmental Microbiology 66: 1050–1056.

    Article  CAS  Google Scholar 

  128. Shelobolina, E., S. Sullivan, K. O‘Neill, K. Nevin, and D. Lovley. 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.. Applied and Environmental Microbiology 70: 2959–2965.

    Article  CAS  Google Scholar 

  129. Caccavo, F., R. Blakemore, and D. Lovley. 1992. A hydrogen-oxidizing, Fe(III)-reducing microorganism from the Great Bay Estuary, New Hampshire. Applied and Environmental Microbiology 58: 3211–3216.

    CAS  Google Scholar 

  130. Roh, Y., S. Liu, G. Li, H. Huang, T. Phelps, and J. Zhou. 2002. Isolation and Characterization of Metal-Reducing Thermoanaerobacter Strains from Deep Subsurface Environments of the Piceance Basin, Colorado. Applied and Environmental Microbiology 68: 6013–6020.

    Article  CAS  Google Scholar 

  131. Kieft, T., J. Fredrickson, T. Onstott, Y. Gorby, H. Kostandarithes, T. Bailey, D. Kennedy, S. Li, A. Plymale, C. Spadoni, and M. Gray. 1999. Dissimilatory reduction of Fe(III) and other electron acceptors by a Thermus isolate. Applied and Environmental Microbiology 65: 1214–1221.

    CAS  Google Scholar 

  132. Khijniak, T., A. Slobodkin, V. Coker, J. Renshaw, F. Livens, E. Bonch-Osmolovskaya, N. Birkeland, N. Medvedeva-Lyalikova, and J. Lloyd. 2005. Reduction of uranium(VI) phosphate during growth of the thermophilic bacterium Thermoterrabacterium ferrireducens. Applied and Environmental Microbiology 71: 6423–6426.

    Article  CAS  Google Scholar 

  133. Elias, D., J. Suflita, M. McInerney, and L. Krumholz. 2004. Periplasmic cytochrome c3 of Desulfovibrio vulgaris is directly involved in H2-mediated metal but not sulfate reduction. Applied and Environmental Microbiology 70: 413–420.

    Article  CAS  Google Scholar 

  134. Heidelberg, J., R. Seshadri, S. Haveman, C. Hemme, I. Paulsen, J. Kolonay, J. Eisen, N. Ward, B. Methe, L. Brinkac, S. Daugherty, R. Deboy, R. Dodson, A. Durkin, R. Madupu, W. Nelson, S. Sullivan, D. Fouts, D. Haft, J. Selengut, J. Peterson, T. Davisen, N. Zafar, L. Zhou, D. Radune, G. Dimitrov, M. Hance, K. Tran, H. Khouri, J. Gill, T. Utterback, T. Feldblyum, J. Wall, G. Voordouw, and C. Fraser. 2004. The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nature Biotechnology 22: 554–559.

    Article  CAS  Google Scholar 

  135. Lovley, D., P. Widman, J. Woodhard, and E. Phillips. 1993. Reduction of uranium by cytochrome c3 of Desulfovibrio vulgaris. Applied and Environmental Microbiology 59: 3572–3576.

    CAS  Google Scholar 

  136. Payne, R., L. Casalot, T. Rivere, J. Terry, L. Larsen, B. Giles, and J. Wall. 2004. Interaction between uranium and the cytochrome c3 of Desulfovibrio desulfuricans strain G20. Archives of Microbiology 181: 398–406.

    Article  CAS  Google Scholar 

  137. Shelobolina, E., M. Coppi, A. Korenevsky, L. Didonato, S. Sullivan, H. Konishi, H. Xu, C. Leang, J. Butler, B. Kim, and D. Lovley. 2007. Importance of c-type cytochromes for U(VI) reduction by Geobacter sulfurreducens. BMC Microbiology 7: 16.

    Article  CAS  Google Scholar 

  138. Heidelberg, J., I. Paulsen, K. Nelson, E. Gaidos, W. Nelson, T. Read, J. Eisen, R. Seshadri, N. Ward, B. Methe, R. Clayton, T. Meyer, A. Tsapin, J. Scott, M. Beanan, L. Brinkac, S. Daugherty, R. Deboy, R. Dodson, A. Durkin, D. Haft, J. Kolonay, R. Madupu, J. Peterson, L. Umayam, O. White, A. Wolf, J. Vamathevan, J. Weidman, M. Impraim, K. Lee, K. Berry, C. Lee, J. Mueller, H. Khouri, J. Gill, T. Utterback, L. McDonald, T. Feldblyum, H. Smith, J. Venter, K. Nealson, and C. Fraser. 2002. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nature Biotechnology 20: 1118–1123.

    Article  CAS  Google Scholar 

  139. Beller, H., T. Legler, F. Bourquet, T. Letain, S. Kane, and M. Coleman. 2009. Identification of c-type cytochromes involved in anaerobic, bacterial U(IV) oxidation. Biodegradation 20: 45–53.

    Article  CAS  Google Scholar 

  140. Merroun, M., J. Raff, A. Rossberg, C. Hennig, T. Reich, and S. Selenska-Pobell. 2005. Complexation of uranium by cells and S-layer sheets of Bacillus sphaericus JG-A12. Applied and Environmental Microbiology 71: 5532–5543.

    Article  CAS  Google Scholar 

  141. Fowle, D., J. Fein, and A. Martin. 2000. Experimental study of uranyl adsorption onto Bacillus subtilis. Environmental Science and Technology 34: 3737–3741.

    Article  CAS  Google Scholar 

  142. Gorman-Lewis, D., P. Elias, and J. Fein. 2005. Adsorption of aqueous uranyl complexes onto Bacillus subtilis cells. Environmental Science and Technology 39: 4906–4912.

    Article  CAS  Google Scholar 

  143. Kelly, S., K. Kemner, J. Fein, D. Fowle, M. Boyanov, B. Bunker, and N. Yee. 2002. X-ray absorption fine structure determination of pH-dependent U-bacterial cell wall interactions. Geochimica et Cosmochimica Acta 65: 3855–3871.

    Article  Google Scholar 

  144. Haas, J., T. Dichristina, and R. Wade. 2001. Thermodynamics of U(VI) sorption onto Shewanella putrefaciens. Chemical Geology 180: 33–54.

    Article  CAS  Google Scholar 

  145. Langley, S., and T. Beveridge. 1999. Effect of O-side-chain-lipopolysaccharide chemistry on metal binding. Applied and Environmental Microbiology 65: 489–498.

    CAS  Google Scholar 

  146. Koban, A., G. Geipel, A. Robberg, and G. Bernhard. 2004. Uranyl (VI) complexes with sugar phosphates in aqueous solution. Radiochimica Acta 92: 903–908.

    Article  CAS  Google Scholar 

  147. Merroun, M., C. Hennig, A. Rossberg, T. Reich, and S. Selenska-Pobell. 2003. Characterization of U(VI)-Acidithiobacillus ferrooxidans complexes by using EXAFS, transmission electron microscopy and energy-dispersive X-ray analysis. Radiochimica Acta 91: 583–591.

    Article  CAS  Google Scholar 

  148. Anderson, R., H. Vrionis, I. Ortiz-Bernad, C. Resch, P. Long, R. Dayvault, K. Karp, S. Marutcky, S. Metzler, A. Peacock, D. White, M. Lowe, and D. Lovley. 2003. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Applied and Environmental Microbiology 69: 5884–5891.

    Article  CAS  Google Scholar 

  149. Chang, Y., P. Long, R. Geyer, A. Peacock, S. Pfiffner, A. Smithgal, R. Anderson, H. Vrionis, J. Stephen, R. Dayvault, I. Ortiz-Bernad, D. Lovley, and D. White. 2005. Microbial incorporation of 13C-labeled acetate at the field scale: detection of microbes responsible for reduction of U(VI. Environmental Science and Technology 39: 9039–9048.

    Article  CAS  Google Scholar 

  150. Yabusaki, S., Y. Fang, P. Long, C. Resch, A. Peacock, J. Komlos, P. Jaffe, S. Morrison, R. Dayvault, D. White, and R. Anderson. 2007. Uranium removal from groundwater via in situ biostimulation: field-scale modeling of transport and biological processes. Journal of Contaminant Hydrology 93: 216–235.

    Article  CAS  Google Scholar 

  151. Istok, J., J. Senko, L. Krumholz, D. Watson, M. Bogle, A. Peacock, Y. Chang, and D. White. 2004. In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer. Environmental Science and Technology 38: 468–475.

    Article  CAS  Google Scholar 

  152. North, N., S. Dollhopf, L. Petrie, J. Istok, D. Balkwill, and J. Kostka. 2004. Change in bacterial community structure during in situ biostimulation of subsurface sediment cocontaminated with uranium and nitrate. Applied and Environmental Microbiology 70: 4911–4920.

    Article  CAS  Google Scholar 

  153. Petrie, L., N. North, S. Dollhopf, D. Balkwill, and J. Kostka. 2003. Enumeration and characterization of iron(III)-reducing microbial communities from acidic subsurface sediments contaminated wih uranium(VI. Applied and Environmental Microbiology 69: 7467–7479.

    Article  CAS  Google Scholar 

  154. Luo, J., O. Cirpka, W. Wu, M. Fienen, P. Jardine, T. Mehlhorn, D. Watson, C. Criddle, and P. Kitanidis. 2005. Mass-transfer limitations for nitrate removal in a uranium-contaminated aquifer. Environmental Science and Technology 39: 8453–8459.

    Article  CAS  Google Scholar 

  155. Wu, W., B. Gu, M. Fields, M. Gentile, Y. Ku, H. Yan, S. Tiquias, T. Yan, J. Nyman, J. Zhou, P. Jardine, and C. Criddle. 2005. Uranium (VI) reduction by denitrifying biomass. Bioremediation Journal 9: 49–61.

    Article  CAS  Google Scholar 

  156. Chinni, S., C. Anderson, K.-U. Ulrich, D. Giammar, and B. Tebo. 2008. Indirect UO2 oxidation by Mn(II)-oxidizing spores of Bacillus sp. strain SG-1 and the effect of U and Mn concentrations. Environmental Science and Technology 42: 8709–8714.

    Article  CAS  Google Scholar 

  157. Zhang, G., J. Senko, S. Kelly, H. Tan, K. Kemner, and W. Burgos. 2009. Microbial reduction of iron(III)-rich nontronite and uranium(VI. Geochimica et Cosmochimica Acta 73: 3523–3538.

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by the Office of Science (BER), U.S. Department of Energy, Grant No. DE-FG02-08ER64560. We thank Raice Ahmad for providing data on uranium immobilization using S. oneidensis MR-1 biofilms and Alice Dohnalkova for HRTEM and SEM biofilm images. We also wish to thank anonymous reviewers for reviewing our manuscript. A portion of this research was performed at the Environmental Molecular Sciences Laboratory (EMSL), a national scientific user facility sponsored by the U.S. Department of Energy’s Office of Biological and Environmental Research and located at Pacific Northwest National Laboratory (PNNL). Beyenal acknowledges Professors Zbigniew Lewandowski and Brent Peyton, Montana State University and DOE (Grants #DE-FG03-98ER62630/A001 and #DE-FG03-01ER63270) for his past training on biofilms and uranium.

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  1. The Gene and Linda Voiland School of Chemical Engineering and Bioengineering and the Center for Environmental, Sediment and Aquatic Research, Washington State University, Pullman, 99163-2710, Washington, DC, USA

    Bin Cao, Bulbul Ahmed & Haluk Beyenal

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  1. Bin Cao
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  2. Bulbul Ahmed
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Correspondence to Haluk Beyenal .

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  1. Dowling College, Idle Hour Blvd. 150, Oakdale, 11769, USA

    Vishal Shah

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Cao, B., Ahmed, B., Beyenal, H. (2010). Immobilization of Uranium in Groundwater Using Biofilms. In: Shah, V. (eds) Emerging Environmental Technologies, Volume II. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3352-9_1

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