About this Journal Submit a Manuscript Table of Contents
ISRN Biotechnology
Volume 2013 (2013), Article ID 657160, 11 pages
http://dx.doi.org/10.5402/2013/657160
Research Article

Fermentation and Hydrogen Metabolism Affect Uranium Reduction by Clostridia

1Center for Biosignatures Discovery Automation, Biodesign Institute, Arizona State University, Tempe, AZ 85287, USA
2Division of Advanced Nuclear Engineering, Pohang University of Science and Technology, Pohang 790-784, Republic of Korea
3Environmental Sciences Department, Brookhaven National Laboratory, Upton, NY 11973, USA

Received 12 December 2012; Accepted 19 January 2013

Academic Editors: V. P. Bulgakov and M. Rossi

Copyright © 2013 Weimin Gao and Arokiasamy J. Francis. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. Cardenas, W. M. Wu, B. M. Leigh et al., “Significant association between sulfate-reducing bacteria and uranium-reducing microbial communities as revealed by a combined massively parallel sequencing-indicator species approach,” Applied and Environmental Microbiology, vol. 76, no. 20, pp. 6778–6786, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. Y. Liang, J. D. Van Nostrand, L. A. N'guessan, et al., “Microbial functional gene diversity with a shift of subsurface redox conditions during in situ uranium reduction,” Applied and Environmental Microbiology, vol. 76, no. 20, pp. 6778–6786, 2012.
  3. J. D. Van Nostrand, L. Wu, W. M. Wu et al., “Dynamics of microbial community composition and function during in situ bioremediation of a uranium-contaminated aquifer,” Applied and Environmental Microbiology, vol. 77, no. 11, pp. 3860–3869, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. J. C. Renshaw, L. J. C. Butchins, F. R. Livens, I. May, J. M. Charnock, and J. R. Lloyd, “Bioreduction of uranium: environmental implications of a pentavalent intermediate,” Environmental Science and Technology, vol. 39, no. 15, pp. 5657–5660, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. J. D. Wall and L. R. Krumholz, “Uranium reduction,” Annual Review of Microbiology, vol. 60, pp. 149–166, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. M. J. Wilkins, F. R. Livens, D. J. Vaughan, and J. R. Lloyd, “The impact of Fe(III)-reducing bacteria on uranium mobility,” Biogeochemistry, vol. 78, no. 2, pp. 125–150, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. S. B. Leschine, “Cellulose degradation in anaerobic environments,” Annual Review of Microbiology, vol. 49, pp. 399–426, 1995. View at Scopus
  8. D. R. Woods, “The genetic engineering of microbial solvent production,” Trends in Biotechnology, vol. 13, no. 7, pp. 259–264, 1995. View at Publisher · View at Google Scholar · View at Scopus
  9. J. G. Zeikus, “Chemical and fuel production by anaerobic bacteria,” Annual Review of Microbiology, vol. 34, pp. 423–464, 1980. View at Scopus
  10. J. S. Chen and J. L. Johnson, “Molecular biology of nitrogen fixation in the clostridia,” Biotechnology, vol. 25, pp. 371–392, 1993. View at Scopus
  11. H. G. Wood and L. G. Ljungdahl, “Autotrophic character of acetogenic bacteria,” in Variations in Autotrophic Life, J. M. Shively and L. L. Barton, Eds., pp. 201–250, Academic Press, San Diego, Calif, USA, 1991.
  12. A. Karnholz, K. Küsel, A. Gößner, A. Schramm, and H. L. Drake, “Tolerance and metabolic response of acetogenicbacteria toward oxygen,” Applied and Environmental Microbiology, vol. 68, pp. 1005–1009, 2002.
  13. K. Küsel, A. Karnholz, T. Trinkwalter, R. Devereux, G. Acker, and H. L. Drake, “Physiological ecology of Clostridium glycolicum RD-1, an aerotolerant acetogen isolated from sea grass roots,” Applied and Environmental Microbiology, vol. 67, no. 10, pp. 4734–4741, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. A. J. Francis, C. J. Dodge, F. Lu, G. P. Halada, and C. R. Clayton, “XPS and XANES studies of uranium reduction by Clostridium sp.,” Environmental Science Technology, vol. 28, no. 4, pp. 636–639, 1994. View at Scopus
  15. A. J. Francis, C. J. Dodge, and G. E. Meinken, “Biotransformation of pertechnetate by Clostridia,” Radiochimica Acta, vol. 90, no. 9–11, pp. 791–797, 2002. View at Scopus
  16. A. J. Francis, G. Joshi-T, C. J. Dodge, and J. B. Gillow, “Biotransformation of uranium and transition metal citrate complexes by Clostridia,” Journal of Nuclear Science and Technology, vol. 3, supplement, pp. 935–938, 2002.
  17. W. Gao and A. J. Francis, “Reduction of uranium(VI) to (IV) by Clostrdia,” Applied and Environmental Microbiology, vol. 74, pp. 4580–4584, 2008.
  18. L. Petrie, N. N. North, S. L. Dollhopf, D. L. Balkwill, and J. E. Kostka, “Enumeration and characterization of iron(III)-reducing microbial communities from acidic subsurface sediments contaminated with uranium(VI),” Applied and Environmental Microbiology, vol. 69, no. 12, pp. 7467–7479, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Suzuki, S. D. Kelly, K. M. Kemner, and J. F. Banfield, “Microbial populations stimulated for hexavalent uranium reduction in uranium mine sediment,” Applied and Environmental Microbiology, vol. 69, no. 3, pp. 1337–1346, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. W. Dong, G. Xie, T. R. Miller et al., “Sorption and bioreduction of hexavalent uranium at a military facility by the Chesapeake Bay,” Environmental Pollution, vol. 142, no. 1, pp. 132–142, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. A. S. Madden, A. C. Smith, D. L. Balkwill, L. A. Fagan, and T. J. Phelps, “Microbial uranium immobilization independent of nitrate reduction,” Environmental Microbiology, vol. 9, no. 9, pp. 2321–2330, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. A. J. Francis and C. J. Dodge, “Anaerobic microbial dissolution of transition and heavy metal oxides,” Applied and Environmental Microbiology, vol. 54, pp. 1009–1014, 1988.
  23. E. R. Weyer and L. F. Rettger, “A comparative study of six different strains of the organism commonly concerned in large-scale production of butyl alcohol and acetone by the biological process,” Journal of Bacteriology, vol. 14, pp. 399–424, 1927.
  24. J. Nölling, G. Breton, M. V. Omelchenko et al., “Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum,” Journal of Bacteriology, vol. 183, no. 16, pp. 4823–4838, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. A. J. Francis, S. Dobbs, and B. J. Nine, “Microbial activity of trench leachates from shallow-land, low-level radioactive waste disposal sites,” Applied and Environmental Microbiology, vol. 40, no. 1, pp. 108–113, 1980. View at Scopus
  26. J. C. Cox, D. G. Nicholls, and W. J. Ingledew, “Transmembrane electrical potential and transmembrane pH gradient in the acidophile Thiobacillus ferrooxidans,” Biochemical Journal, vol. 178, no. 1, pp. 195–200, 1979. View at Scopus
  27. P. D. Cotter and C. Hill, “Surviving the acid test: responses of gram-positive bacteria to low pH,” Microbiology and Molecular Biology Reviews, vol. 67, no. 3, pp. 429–453, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Goodwin and J. G. Zeikus, “Physiological adaptations of anaerobic bacteria to low pH: metabolic control of proton motive force in Sarcina ventriculi,” Journal of Bacteriology, vol. 169, no. 5, pp. 2150–2157, 1987. View at Scopus
  29. A. B. Leaphart, D. K. Thompson, K. Huang et al., “Transcriptome profiling of Shewanella oneidensis gene expression following exposure to acidic and alkaline pH,” Journal of Bacteriology, vol. 188, no. 4, pp. 1633–1642, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. J. D. Istok, J. M. Senko, L. R. Krumholz et al., “In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer,” Environmental Science and Technology, vol. 38, no. 2, pp. 468–475, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. V. M. Fernandez, M. L. Rua, P. Reyes, R. Cammack, and E. C. Hatchikian, “Inhibition of Desulfovibrio gigas hydrogenase with copper salts and other metal ions,” European Journal of Biochemistry, vol. 185, no. 2, pp. 449–454, 1989. View at Scopus
  32. D. A. Elias, J. M. Suflita, M. J. McInerney, and L. R. Krumholz, “Periplasmic cytochrome c3 of desulfovibrio vulgaris Is directly involved in H2-mediated metal but not sulfate reduction,” Applied and Environmental Microbiology, vol. 70, no. 1, pp. 413–420, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. V. N. Yarlagadda, A. Gupta, C. J. Dodge, and A. J. Francis, “Effect of exogenous electron shuttles on growth and fermentative metabolism in Clostridium sp. BC1,” Bioresource Technology, vol. 108, pp. 295–299, 2012.
  34. L. E. Mortenson, “Purification and analysis of ferredoxin from Clostridium pasteurianum,” Biochimica et Biophysica Acta, vol. 81, no. 1, pp. 71–77, 1964. View at Scopus
  35. G. Voordouw and S. Brenner, “Nucleotide sequence of the gene encoding the hydrogenase from Desulfovibrio vulgaris (Hildenborough),” European Journal of Biochemistry, vol. 148, no. 3, pp. 515–520, 1985. View at Scopus
  36. G. Voordouw, J. D. Strang, and F. R. Wilson, “Organization of the genes encoding [Fe] hydrogenase in Desulfovibrio vulgaris,” Journal of Bacteriology, vol. 171, no. 7, pp. 3881–3889, 1989. View at Scopus
  37. T. Happe, B. Mosler, and J. D. Naber, “Induction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii,” European Journal of Biochemistry, vol. 222, no. 3, pp. 769–774, 1994. View at Publisher · View at Google Scholar · View at Scopus
  38. M. J. Payne, A. Chapman, and R. Cammack, “Evidence for an [Fe]-type hydrogenase in the parasitic protozoan Trichomonas vaginalis,” FEBS Letters, vol. 317, no. 1-2, pp. 101–104, 1993. View at Publisher · View at Google Scholar · View at Scopus
  39. M. C. Posewitz, P. W. King, S. L. Smolinski, L. Zhang, M. Seibert, and M. L. Ghirardi, “Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase,” Journal of Biological Chemistry, vol. 279, no. 24, pp. 25711–25720, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. M. W. W. Adams, “The structure and mechanism of iron-hydrogenases,” Biochimica et Biophysica Acta, vol. 1020, no. 2, pp. 115–145, 1990. View at Publisher · View at Google Scholar · View at Scopus
  41. J. W. Peters, “X-ray crystal structure of the Fe-only hydrogenase (Cpl) from Clostridium pasteurianum to 1.8 angstrom resolution,” Science, vol. 282, no. 5395, pp. 1853–1858, 1998. View at Scopus
  42. M. J. Marshall, A. E. Plymale, D. W. Kennedy et al., “Hydrogenase- and outer membrane c-type cytochrome-facilitated reduction of technetium(VII) by Shewanella oneidensis MR-1,” Environmental Microbiology, vol. 10, no. 1, pp. 125–136, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Shi, D. J. Richardson, Z. Wang et al., “The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer,” Environmental Microbiology Reports, vol. 1, no. 4, pp. 220–227, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Gottwald, J. R. Andreesen, J. LeGall, and L. G. Ljungdahl, “Presence of cytochrome and menaquinone in Clostridium formicoaceticum and Clostridium thermoaceticum,” Journal of Bacteriology, vol. 122, no. 1, pp. 325–328, 1975. View at Scopus
  45. E. D. Vecchia, H. Veeramani, E. I. Suvorova, N. S. Wigginton, J. R. Bargar, and R. Bernier-Latmani, “U(VI) reduction by spores of Clostridium acetobutylicum,” Research in Microbiology, vol. 161, no. 9, pp. 765–771, 2010. View at Publisher · View at Google Scholar · View at Scopus