Direct and Indirect Processes Leading to Uranium(IV) Oxidation

Rizlan Bernier-Latmani; Bradley M. Tebo

doi:10.1128/9781555817190.ch8

Chapter 8 : Direct and Indirect Processes Leading to Uranium(IV) Oxidation

Authors: Rizlan Bernier-Latmani¹, Bradley M. Tebo²

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Environmental Microbiology Laboratory, Ecole Polytechnique Fédérale de Lausanne, CH 1015 Lausanne, Switzerland; 2: Division of Environmental and Biomolecular Systems, Oregon Health & Science University, Beaverton, OR 97006

Content Type: Monograph

Publication Year: 2011

Category: Applied and Industrial Microbiology; Environmental Microbiology

Book DOI: 10.1128/9781555817190

Chapter DOI: 10.1128/9781555817190.ch8

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Direct and Indirect Processes Leading to Uranium(IV) Oxidation, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555817190/9781555815363_Chap08-1.gif /docserver/preview/fulltext/10.1128/9781555817190/9781555815363_Chap08-2.gif

Abstract:

Microbial activity has shown to catalyze the reduction of the soluble and mobile contaminant uranium (VI) to the sparingly soluble, nanoparticulate mineral uraninite (UO2). Many of the oxidants can be formed biologically, and these various redox-active compounds can also react with each other. Thus, the potential oxidation of uranium (IV) in the subsurface is a complex and intricate series of direct and indirect coupled biological redox reactions. This chapter presents a comprehensive view of the collective understanding of the processes potentially responsible for uranium (IV) oxidation in the subsurface. Most studies have focused on the most widely reported product of microbial U(VI) reduction, namely the mineral uraninite. In particular, the comparison of two studies allows an evaluation of the effect of sulfate on the reoxidation of U(IV) by oxygen. Although the studies focused on the abiotic oxidation of U(IV) by molecular oxygen, a single study reported the aerobic and enzymatic oxidation of U(IV). Accounting for this catalytic UO2 oxidation coupled to Mn, cycling is needed to evaluate the long-term stability of U(IV) at remediated sites. A major aspect of the mechanism(s) of abiotic U(IV) oxidation by Fe(III) and Mn(III,IV) oxides remains poorly understood: both reactants are solid phases and it is unclear how the relative localization of the two minerals influences the U(IV) oxidation.

Citation: Bernier-Latmani R, Tebo B. 2011. Direct and Indirect Processes Leading to Uranium(IV) Oxidation, p 138-156. In Stolz J, Oremland R (ed), Microbial Metal and Metalloid Metabolism. ASM Press, Washington, DC. doi: 10.1128/9781555817190.ch8

Highlighted Text: Show | Hide

Full text loading...

Figures

Direct and Indirect Processes Leading to Uranium(IV) Oxidation

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817190.ch08-1,webId=/content/author/10.1128/9781555817190.ch08-1,properties={foaf_givenname=Rizlan, foaf_name=Rizlan Bernier-Latmani, foaf_surname=Bernier-Latmani, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817190.ch08-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817190.ch08-2,webId=/content/author/10.1128/9781555817190.ch08-2,properties={foaf_givenname=Bradley M., foaf_name=Bradley M. Tebo, foaf_surname=Tebo, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817190.ch08-aff2]]}]]

/content/10.1128/9781555817190.ch08.ch08fig01

FIGURE 1

High-resolution transmission electron microscopy (HRTEM) (left) and Fourier-filtered HRTEM (right) image of biogenic nanoparticles of UO2 obtained from S. oneidensis MR-1 under nongrowth conditions. 10.1128/9781555817190.ch8.f1

10.1128/9781555817190/f0140-01_thmb.gif

10.1128/9781555817190/f0140-01.gif

FIGURE 1

/content/10.1128/9781555817190.ch08.ch08fig02

FIGURE 2

Redox potentials of species discussed in the text. Thermodynamic data were obtained from Ginder-Vogel et al. (2006 ) and Morel and Hering (1993 ). All calculations were carried out at pH 7. 10.1128/9781555817190.ch8.f2

10.1128/9781555817190/f0141-01_thmb.gif

10.1128/9781555817190/f0141-01.gif

FIGURE 2

/content/10.1128/9781555817190.ch08.ch08fig03

FIGURE 3

Schematic of the direct and indirect biological pathways involving oxygen for U(IV) oxidation. In this and subsequent figures, the boxed text corresponds to the electron acceptor in the processes considered. 10.1128/9781555817190.ch8.f3

10.1128/9781555817190/f0142-01_thmb.gif

10.1128/9781555817190/f0142-01.gif

FIGURE 3

/content/10.1128/9781555817190.ch08.ch08fig04

FIGURE 4

Schematic of the direct and indirect biological pathways involving N oxides for U(IV) oxidation. The product of nitrite reduction by U(IV) is taken to be NO2 – ( Senko et al., 2005a ) by analogy to Fe(II) ( Cooper et al., 2003 ). Only NO2 – was considered as the product of heterotrophic denitrification for the sake of simplicity. In reality, N2O and NO are also formed and also oxidize U(IV) abiotically (especially N2O). For the anaerobic U(IV) oxidizer, the bacterium is capable of complete denitrification, but this was not measured (H. Beller, personal communication). In this and subsequent figures, dashed and shaded boxes are intended for purely aesthetic reasons to aid in the visual separation of the various processes in the diagram. 10.1128/9781555817190.ch8.f4

10.1128/9781555817190/f0144-01_thmb.gif

10.1128/9781555817190/f0144-01.gif

FIGURE 4

/content/10.1128/9781555817190.ch08.ch08fig05

FIGURE 5

Schematic of the direct and indirect biological pathways involving iron oxides for U(IV) oxidation. The product of coupled Fe(II) oxidation and nitrate reduction is most commonly N2 ( Straub et al., 2001 ). Fe(III) labeled in bold corresponds to the most reactive form of Fe(III) produced by the processes considered. 10.1128/9781555817190.ch8.f5

10.1128/9781555817190/f0148-01_thmb.gif

10.1128/9781555817190/f0148-01.gif

FIGURE 5

/content/10.1128/9781555817190.ch08.ch08fig06

FIGURE 6

Schematic of the direct and indirect biological pathways involving Mn oxides for U(IV) oxidation. 10.1128/9781555817190.ch8.f6

10.1128/9781555817190/f0151-01_thmb.gif

10.1128/9781555817190/f0151-01.gif

FIGURE 6

Schematic of the direct and indirect biological pathways involving Mn oxides for U(IV) oxidation. 10.1128/9781555817190.ch8.f6

References

/content/book/10.1128/9781555817190.ch08

1. Abdelouas, A.,, W. Lutze, and, H. E. Nuttall. 1999. Oxidative dissolution of uraninite precipitated on Navajo Sandstone. J. Contam. Hydrol. 36: 353– 375.

2. Allen, G. C.,, and P. A. Tempest. 1986. Ordered defects in the oxides of uranium. Proc. R. Soc. Lond. Ser. A 406: 325– 344.

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

4. Bargar, J. R.,, R. Bernier-Latmani,, D. E. Giammar, and, B. M. Tebo. 2008. Biogenic uraninite nanoparticles and their importance for uranium remediation. Elements 4: 407– 412.

5. Bargar, J. R.,, B. M. Tebo,, U. Bergmann,, S. M. Webb,, P. Glatzel,, V. Q. Chiu, and, M. Villalobos. 2005. Biotic and abiotic products of Mn(II) oxidation by spores of the marine Bacillus sp. strain SG-1. Am. Mineral. 90: 143– 154.

6. Bartlett, R.,, and B. James. 1979. Behavior of chromium in soils. 3. Oxidation. J. Environ. Qual. 8: 31– 35.

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

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

9. Boyanov, M. I.,, E. J. O’Loughlin,, E. E. Roden,, J. B. Fein, and, K. M. Kemner. 2007. Adsorption of Fe(II) and U(VI) to carboxyl-functionalized microspheres: the influence of speciation on uranyl reduction studied by titration and XAFS. Geochim. Cosmochim. Acta 71: 1898– 1912.

10. Burgos, W. D.,, J. T. McDonough,, J. M. Senko,, G. X. Zhang,, A. C. Dohnalkova,, S. D. Kelly,, Y. Gorby, and, K. M. Kemner. 2008. Characterization of uraninite nanoparticles produced by Shewanella oneidensis MR-1. Geochim. Cosmochim. Acta 72: 4901– 4915.

11. Chinni, S.,, C. R. Anderson,, K. U. Ulrich,, D. E. Giammar, and, B. M. Tebo. 2008. Indirect UO 2 oxidation by Mn(II)-oxidizing spores of Bacillus sp. strain SG-1 and the effect of U and Mn concentrations. Environ. Sci. Technol. 42: 8709– 8714.

12. Clement, B. G.,, G. W. Luther, and, B. M. Tebo. 2009. Rapid, oxygen-dependent microbial Mn(II) oxidation kinetics at sub-micromolar oxygen concentrations in the Black Sea suboxic zone. Geochim. Cosmochim. Acta 73: 1878– 1889.

13. Cooper, D. C.,, F. W. Picardal,, A. Schimmelmann, and, A. J. Coby. 2003. Chemical and biological interactions during nitrate and goethite reduction by Shewanella putrefaciens 200. Appl. Environ. Microbiol. 69: 3517– 3525.

14. DiSpirito, A. A.,, and O. H. Tuovinen. 1982. Uranous ion oxidation and carbon dioxide fixation by Thiobacillus ferroxidans. Arch. Microbiol. 133: 28– 32.

15. Fendorf, S.,, P. M. Jardine,, R. R. Patterson,, D. L. Taylor, and, S. C. Brooks. 1999. Pyrolusite surface transformations measured in real-time during the reactive transport of Co(II)EDTA (2-). Geochim. Cosmochim. Acta 63: 3049– 3057.

16. Finch, R. J.,, and T. Murakami. 1999. Systematics and paragenesis of uranium minerals. Rev. Mineral. Geochem. 38: 91– 179.

17. Finneran, K. T.,, M. E. Housewright, and, D. R. Lovley. 2002. Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments. Environ. Microbiol. 4: 510– 516.

18. Francis, A. J.,, C. J. Dodge,, F. Lu,, G. P. Halada, and, C. R. Clayton. 1994. XPS and XANES studies of uranium reduction by Clostridium sp. Environ. Sci. Technol. 28: 636– 639.

19. Fredrickson, J. K.,, J. M. Zachara,, D. W. Kennedy,, C. Liu,, M. C. Duff,, D. B. Hunter, and, A. Dohnalkona. 2002. Influence of Mn oxides on the reduction of U(VI) by the metal-reducing bacterium Shewanella putrefaciens. Geochim. Cosmochim. Acta 66: 3247– 3262.

20. Ginder-Vogel, M.,, C. S. Criddle, and, S. Fendorf. 2006. Thermodynamic constraints on the oxidation of biogenic UO 2 by Fe(III) (hydr) oxides. Environ. Sci. Technol. 40: 3544– 3550.

21. Ginder-Vogel, M.,, B. Stewart, and, S. Fendorf. 2010. Kinetic and mechanistic constraints on the oxidation of biogenic uraninite by ferrihydrite. Environ. Sci. Technol. 44: 163– 169.

22. Gu, B. H.,, H. Yan,, P. Zhou,, D. B. Watson,, M. Park, and, J. Istok. 2005. Natural humics impact uranium bioreduction and oxidation. Environ. Sci. Technol. 39: 5268– 5275.

23. Istok, J. D.,, J. M. Senko,, L. R. Krumholz,, D. Watson,, M. A. Bogle,, A. Peacok,, Y.-J. Chang, and, D. C. White. 2004. In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer. Environ. Sci. Technol. 38: 468– 475.

24. Janeczek, J.,, and R. C. Ewing. 1992. Structural formula of uraninite. J. Nucl. Mater. 190: 128– 132.

25. Komlos, J.,, A. Peacock,, R. K. Kukkadapu, and, P. R. Jaffe. 2008. Long-term dynamics of uranium reduction/reoxidation under low sulfate conditions. Geochim. Cosmochim. Acta 72: 3603– 3615.

26. Letain, T. E.,, S. R. Kane,, T. C. Legler,, E. P. Salazar,, P. G. Agron, and, H. R. Beller. 2007. Development of a genetic system for the chemolithoautotrophic bacterium Thiobacillus denitrificans. Appl. Environ. Microbiol. 73: 3265– 3271.

27. Liger, E.,, L. Charlet, and, P. Van Cappellen. 1999. Surface catalysis of uranium(VI) reduction by iron(II). Geochim. Cosmochim. Acta 63: 2939– 2955.

28. Liu, C. X.,, J. M. Zachara,, J. K. Fredrickson,, D. W. Kennedy, and, A. Dohnalkova. 2002. Modeling the inhibition of the bacterial reduction of U(VI) by β-MnO 2(s). Environ. Sci. Technol. 36: 1452– 1459.

29. Lovley, D. R. 1993. Dissimilatory metal reduction. Annu. Rev. Microbiol. 47: 263– 290.

30. Lovley, D. R.,, E. J. P. Phillips,, Y. A. Gorby, and, E. R. Landa. 1991. Microbial reduction of uranium. Nature 350: 413– 416.

31. Moon, H. S.,, J. Komlos, and, P. R. Jaffe. 2007. Uranium reoxidation in previously bioreduced sediment by dissolved oxygen and nitrate. Environ. Sci. Technol. 41: 4587– 4592.

32. Moon, H. S.,, J. Komlos, and, P. R. Jaffe. 2009. Biogenic U(IV) oxidation by dissolved oxygen and nitrate in sediment after prolonged U(VI)/Fe(III)/SO 4 2– reduction. J. Contam. Hydrol. 105: 18– 27.

33. Morel, F. M. M.,, and J. G. Hering. 1993. Principles and Applications of Aquatic Chemistry. John Wiley & Sons, New York, NY.

34. Murray, K. J.,, and B. M. Tebo. 2007. Cr(III) is indirectly oxidized by the Mn(II)-oxidizing bacterium Bacillus sp strain SG-1. Environ. Sci. Technol. 41: 528– 533.

35. Nevin, K. P.,, and D. R. Lovley. 2000. Potential for nonenzymatic reduction of Fe(III) via electron shuttling in subsurface sediments. Environ. Sci. Technol. 34: 2472– 2478.

36. O’Loughlin, E. J.,, S. D. Kelly,, R. E. Cook,, R. Csencsits, and, K. M. Kemner. 2003. Reduction of uranium(VI) by mixed iron(II)/iron(III) hydroxide (green rust): formation of UO 2 nanoparticles. Environ. Sci. Technol. 37: 721– 727.

37. O’Loughlin, E. J.,, S. D. Kelly, and, K. M. Kemner. 2010. XAFS investigation of the interactions of U VI with secondary mineralization products from the bioreduction of (Fe III) oxides. Environ. Sci. Technol. 44: 1656– 1661.

38. Postma, D.,, and C. A. J. Appelo. 2000. Reduction of Mn-oxides by ferrous iron in a flow system: column experiment and reactive transport modeling. Geochim. Cosmochim. Acta 64: 1237– 1247.

39. Regenspurg, S.,, D. Schild,, T. Schafer,, F. Huber, and, M. E. Malmstrom. 2009. Removal of uranium(VI) from the aqueous phase by iron(II) minerals in presence of bicarbonate. Appl. Geochem. 24: 1617– 1625.

40. Sani, R. K.,, B. M. Peyton,, A. Dohnalkova, and, J. E. Amonette. 2005. Reoxidation of reduced uranium with iron(III) (hydr)oxides under sulfate reducing conditions. Environ. Sci. Technol. 39: 2059– 2066.

41. Schofield, E. J.,, H. Veeramani,, J. O. Sharp,, E. Suvorova,, R. Bernier-Latmani,, A. Mehta,, J. Stahlman,, S. M. Webb,, D. L. Clark,, S. D. Conradson,, E. S. Ilton, and, J. R. Bargar. 2008. Structure of biogenic uraninite produced by Shewanella oneidensis strain MR-1. Environ. Sci. Technol. 42: 7898– 7904.

42. Schroeder, D. C.,, and G. F. Lee. 1975. Potential transformations of chromium in natural waters. Water Air Soil Pollut. 4: 355– 365.

43. Senko, J. M.,, J. D. Istok,, J. M. Suflita, and, L. R. Krumholtz. 2002. In-situ evidence for uranium immobilization and remobilization. Environ. Sci. Technol. 36: 1491– 1496.

44. Senko, J. M.,, S. D. Kelly,, A. C. Dohnalkova,, J. T. Mcdonough,, K. M. Kemner, and, W. D. Burgos. 2007. The effect of U(VI) bioreduction kinetics on subsequent reoxidation of biogenic U(IV). Geochim. Cosmochim. Acta 71: 4644– 4654.

45. Senko, J. M.,, Y. Mohamed,, T. A. Dewers, and, L. R. Krumholz. 2005a. Role for Fe(III) minerals in nitrate-dependent microbial U(IV) oxidation. Environ. Sci. Technol. 39: 2529– 2536.

46. Senko, J. M.,, J. M. Suflita and, L. R. Krumholz. 2005b. Geochemical controls on microbial nitrate-dependent U(IV) oxidation. Geomicrobiol. J. 22: 371– 378.

47. Sharp, J. O.,, E. J. Schofield,, H. Veeramani,, E. I. Suvorova,, D. W. Kennedy,, M. J. Marshall,, A. Mehta,, J. R. Bargar, and, R. Bernier-Latmani. 2009. Structural similarities between biogenic uraninites produced by phylogenetically and metabolically diverse bacteria. Environ. Sci. Technol. 43: 8295– 8301.

48. Straub, K. L.,, M. Benz, and, B. Schink. 2001. Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiol. Ecol. 34: 181– 186.

49. Tebo, B. M.,, J. R. Bargar,, B. G. Clement,, G. J. Dick,, K. J. Murray,, D. Parker,, R. Verity, and, S. M. Webb. 2004. Biogenic manganese oxides: properties and mechanisms of formation. Annu. Rev. Earth Planet. Sci. 32: 287– 328.

50. Tebo, B. M.,, and A. Y. Obraztsova. 1998. Sulfatereducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. FEMS Microbiol. Lett. 162: 193– 198.

51. Tokunaga, T. K.,, J. M. Wan,, Y. M. Kim,, S. R. Sutton,, M. Newville,, A. Lanzirotti, and, W. Rao. 2008. Real-time X-ray absorption spectroscopy of uranium, iron, and manganese in contaminated sediments during bioreduction. Environ. Sci. Technol. 42: 2839– 2844.

52. Ulrich, K.-U.,, E. S. Ilton,, H. Veeramani,, J. O. Sharp,, R. Bernier-Latmani,, E. J. Schofield,, J. R. Bargar, and, D. E. Giammar. 2009. Comparative dissolution kinetics of biogenic and chemogenic uraninite under oxidizing conditions in the presence of carbonate. Geochim. Cosmochim. Acta 73: 6065– 6083.

53. Ulrich, K. U.,, A. Singh,, E. J. Schofield,, J. R. Bargar,, H. Veeramani,, J. O. Sharp,, R. Bernier-Latmani, and, D. E. Giammar. 2008. Dissolution of biogenic and synthetic UO 2 under varied reducing conditions. Environ. Sci. Technol. 42: 5600– 5606.

54. Villalobos, M.,, B. Toner,, J. Bargar, and, G. Sposito. 2003. Characterization of the manganese oxide produced by Pseudomonas putida strain MnB1. Geochim. Cosmochim. Acta 67: 2649– 2662.

55. Webb, S. M.,, C. C. Fuller,, B. M. Tebo, and, J. R. Bargar. 2006. Determination of uranyl incorporation into biogenic manganese oxides using X-ray absorption spectroscopy and scattering. Environ. Sci. Technol. 40: 771– 777.

56. Wersin, P.,, M. F. Hochella,, P. Persson,, G. D. Redden,, J. O. Leckie, and, D. W. Harris. 1994. Interaction between aqueous uranium(VI) and sulfide minerals: spectroscopic evidence for sorption and reduction. Geochim. Cosmochim. Acta 58: 2829– 2843.

57. Wu, Q.,, R. A. Sanford, and, F. E. Loffler. 2006a. Uranium(VI) reduction by Anaeromyxobacter dehalogenans strain 2CP-C. Appl. Environ. Microbiol. 72: 3608– 3614.

58. Wu, W. M.,, J. Carley,, T. Gentry,, M. A. Ginder-Vogel,, M. Fienen,, T. Mehlhorn,, H. Yan,, S. Caroll,, M. N. Pace,, J. Nyman,, J. Luo,, M. E. Gentile,, M. W. Fields,, R. F. Hickey,, B. H. Gu,, D. Watson,, O. A. Cirpka,, J. Z. Zhou,, S. Fendorf,, P. K. Kitanidis,, P. M. Jardine, and, C. S. Criddle. 2006b. 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.

59. Wu, W. M.,, J. Carley,, J. Luo,, M. A. Ginder-Vogel,, E. Cardenas,, M. B. Leigh,, C. C. Hwang,, S. D. Kelly,, C. M. Ruan,, L. Y. Wu,, J. Van Nostrand,, T. Gentry,, K. Lowe,, T. Mehlhorn,, S. Carroll,, W. S. Luo,, M. W. Fields,, B. H. Gu,, D. Watson,, K. M. Kemner,, T. Marsh,, J. Tiedje,, J. Z. Zhou,, S. Fendorf,, P. K. Kitanidis,, P. M. Jardine, and, C. S. Criddle. 2007. In situ bioreduction of uranium(VI) to submicromolar levels and reoxidation by dissolved oxygen. Environ. Sci. Technol. 41: 5716– 5723.

60. Zhong, L. R.,, C. X. Liu,, J. M. Zachara,, D. W. Kennedy,, J. E. Szecsody, and, B. Wood. 2005. Oxidative remobilization of biogenic uranium(IV) precipitates: effects of iron(II) and pH. J. Environ. Qual. 34: 1763– 1771.