Table of Contents Author Guidelines Submit a Manuscript
International Journal of Microbiology
Volume 2010 (2010), Article ID 319527, 9 pages
http://dx.doi.org/10.1155/2010/319527
Review Article

Carbon Monoxide as an Electron Donor for the Biological Reduction of Sulphate

1Laboratory of Microbiology of Anthropogenic Environments, Winogradsky Institute of Microbiology, Russian Academy of Sciences, 117312, prosp. 60 let Oktyabrya, 7, b.2, Moscow, Russia
2Laboratory of Chemical and Environmental Engineering (LEQUIA), University of Girona, 17071 Girona, Spain
3Laboratory of Microbiology, Wageningen University, 6703 HB, Wageningen, The Netherlands

Received 1 October 2009; Revised 10 March 2010; Accepted 31 March 2010

Academic Editor: Michael J. McInerney

Copyright © 2010 Sofiya N. Parshina et al. 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. J. R. Postgate, The Sulphate-Reducing Bacteria, Cambridge University, Cambridge, UK, 1979.
  2. G. Muyzer and A. J. M. Stams, “The ecology and biotechnology of sulphate-reducing bacteria,” Nature Reviews Microbiology, vol. 6, no. 6, pp. 441–454, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. B. Ollivier, R. Cord-Ruwisch, E. C. Hatchikian, and J. L. Garcia, “Characterization of Desulfovibrio fructosovorans sp. nov,” Archives of Microbiology, vol. 149, no. 5, pp. 447–450, 1988. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Sass, H. Rutters, H. Cypionka, and H. Sass, “Desulfobulbus mediterraneus sp. nov., a sulphate-reducing bacterium growing on mono- and disaccharides,” Archives of Microbiology, vol. 177, pp. 468–474.
  5. S. Baena, M.-L. Fardeau, M. Labat, B. Ollivier, J.-L. Garcia, and B. K. C. Patel, “Desulfovibrio aminophilus sp. nov., a novel amino acid degrading and sulfate reducing bacterium from an anaerobic dairy wastewater lagoon,” Systematic and Applied Microbiology, vol. 21, no. 4, pp. 498–504, 1998. View at Google Scholar · View at Scopus
  6. A. J. M. Stams, T. A. Hansen, and G. W. Skyring, “Utilization of amino acids as energy substrates by two marine Desulfovibrio strains,” FEMS Microbiology Ecology, vol. 31, no. 1, pp. 11–15, 1985. View at Publisher · View at Google Scholar · View at Scopus
  7. F. Widdel and T. A. Hansen, “The dissimilatory sulfate- and sulfurreducing bacteria,” in The Prokaryotes, A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer, Eds., pp. 583–624, Springer, Berlin, Germany, 2nd edition, 1992. View at Google Scholar
  8. R. Klemps, H. Cypionka, F. Widdel, and N. Pfennig, “Growth with hydrogen, and further physiological characteristics of Desulfotomaculum species,” Archives of Microbiology, vol. 143, no. 2, pp. 203–208, 1985. View at Google Scholar · View at Scopus
  9. H. J. Nanninga and J. C. Gottschal, “Properties of Desulfovibrio carbinolicus sp. nov. and other sulfate-reducing bacteria isolated from an anaerobic-purification plant,” Applied and Environmental Microbiology, vol. 53, no. 4, pp. 802–809, 1987. View at Google Scholar · View at Scopus
  10. T. N. Nazina, A. E. Ivanova, L. P. Kanchaveli, and E. P. Rozanova, “A new sporeforming thermophilic methylotrophic sulfate-reducing bacterium, Desulfotomaculum kuznetsovii sp. nov.,” Mikrobiologia, vol. 57, pp. 823–827, 1988 (Russian). View at Google Scholar
  11. T. N. Nazina, T. P. Turova, A. B. Poltaraus et al., “Phylogenetic position and chemotaxonomic characteristics of the thermophilic sulfate-reducing bacterium Desulfotomaculum kuznetsovii,” Mikrobiologiya, vol. 68, no. 1, pp. 92–99, 1999. View at Google Scholar
  12. S. N. Parshina, S. Kijlstra, A. M. Henstra, J. Sipma, C. M. Plugge, and A. J. M. Stams, “Carbon monoxide conversion by thermophilic sulfate-reducing bacteria in pure culture and in co-culture with Carboxydothermus hydrogenoformans,” Applied Microbiology and Biotechnology, vol. 68, no. 3, pp. 390–396, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. S. N. Parshina, J. Sipma, Y. Nakashimada et al., “Desulfotomaculum carboxydivorans sp. nov., a novel sulfate-reducing bacterium capable of growth at 100% CO,” International Journal of Systematic and Evolutionary Microbiology, vol. 55, no. 5, pp. 2159–2165, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. A. M. Henstra, C. Dijkema, and A. J. M. Stams, “Archaeglobus fulgidus couples CO oxidation to sulfate reduction and acetogenesis with transietnt formate accumulation,” Environmental Microbiology, vol. 9, pp. 1836–1841, 2007. View at Google Scholar
  15. Y. Tanimoto and F. Bak, “Anaerobic degradation of methylmercaptan and dimethyl sulfide by newly isolated thermophilic sulfate-reducing bacteria,” Applied and Environmental Microbiology, vol. 60, no. 7, pp. 2450–2455, 1994. View at Google Scholar · View at Scopus
  16. F. Aeckersberg, F. A. Rainey, and F. Widdel, “Growth, natural relationships, cellular fatty acids and metabolic adaptation of sulfate-reducing bacteria that utilize long-chain alkanes under anoxic conditions,” Archives of Microbiology, vol. 170, no. 5, pp. 361–369, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. C. M. So and L. Y. Young, “Isolation and characterization of a sulfate-reducing bacterium that anaerobically degrades alkanes,” Applied and Environmental Microbiology, vol. 65, no. 7, pp. 2969–2976, 1999. View at Google Scholar · View at Scopus
  18. I. A. Davidova, K. E. Duncan, O. K. Choi, and J. M. Suflita, “Desulfoglaeba alkanexedens gen. nov., sp. nov. an n-alkane-degrading, sulfate-reducing bacterium,” International Journal of Systematic and Evolutionary Microbiology, vol. 56, no. 12, pp. 2737–2742, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Cravo-Laureau, R. Matheron, J.-L. Cayol, C. Joulian, and A. Hirschler-Réa, “Desulfatibacillum aliphaticivorans gen. nov., sp. nov., an n-alkane- and n-alkene-degrading, sulfate-reducing bacterium,” International Journal of Systematic and Evolutionary Microbiology, vol. 54, no. 1, pp. 77–83, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. V. Grossi, C. Cravo-Laureau, A. Meóu, D. Raphel, F. Garzino, and A. Hirschler-Réa, “Anaerobic 1-alkene metabolism by the alkane- and alkene-degrading sulfate reducer Desulfatibacillum aliphaticivorans strain CV2803T,” Applied and Environmental Microbiology, vol. 73, no. 24, pp. 7882–7890, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. O. Kniemeyer, F. Musat, S. M. Sievert et al., “Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria,” Nature, vol. 449, no. 7164, pp. 898–901, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Schnell, F. Bak, and N. Pfennig, “Anaerobic degradation of aniline and dihydroxybenzenes by newly isolated sulfate-reducing bacteria and description of Desulfobacterium anilini,” Archives of Microbiology, vol. 152, no. 6, pp. 556–563, 1989. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Rabus, R. Nordhaus, W. Ludwig, and F. Widdel, “Complete oxidation of toluene under strictly anoxic conditions by a new sulfate-reducing bacterium,” Applied and Environmental Microbiology, vol. 59, no. 5, pp. 1444–1451, 1993. View at Google Scholar · View at Scopus
  24. G. Harms, K. Zengler, R. Rabus et al., “Anaerobic oxidation of o-xylene, m-xylene, and homologous alkylbenzenes by new types of sulfate-reducing bacteria,” Applied and Environmental Microbiology, vol. 65, no. 3, pp. 999–1004, 1999. View at Google Scholar · View at Scopus
  25. B. Morasch, B. Schink, C. C. Tebbe, and R. U. Meckenstock, “Degradation of o-xylene and m-xylene by a novel sulfate-reducer belonging to the genus Desulfotomaculum,” Archives of Microbiology, vol. 181, no. 6, pp. 407–417, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Schink and M. Friedrich, “Phosphite oxidation by sulphate reduction,” Nature, vol. 406, no. 6791, p. 37, 2000. View at Google Scholar · View at Scopus
  27. P. N. L. Lens, A. Visser, A. J. H. Janssen, L. W. Hulshoff Pol, and G. Lettinga, “Biotechnological treatment of sulfate-rich wastewaters,” Critical Reviews in Environmental Science and Technology, vol. 28, no. 1, pp. 41–88, 1998. View at Publisher · View at Google Scholar · View at Scopus
  28. A. J. H. Janssen, H. Dijkman, and G. Janssen, “Novel biological processes for the removal of H2S and SO2 from gas streams,” in Environmental Technologies to Treat Sulfur Pollutions; Principles and Engineering, P. N. L. Lens and L. W. Hulshoff Pol, Eds., pp. 265–280, IWA Publishing, London, UK, 2000. View at Google Scholar
  29. B. H. G. W. van Houten, K. Roest, V. A. Tzeneva, H. Dijkman, H. Smidt, and A. J. M. Stams, “Occurrence of methanogenesis during start-up of a full-scale synthesis gas-fed reactor treating sulfate and metal-rich wastewater,” Water Research, vol. 40, no. 3, pp. 553–560, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Johnson, “Biological removal of sulfurous compounds from inorganic wastewaters,” in Environmental Technologies to Treat Sulfur Pollutions; Principles and Engineering, P. N. L. Lens and L. W. Hulshoff Pol, Eds., pp. 175–205, IWA Publishing, London, UK, 2000. View at Google Scholar
  31. R. T. van Houten, L. W. Hulshoff Pol, and G. Lettinga, “Biological sulphate reduction using gas-lift reactors fed with hydrogen and carbon dioxide as energy and carbon source,” Biotechnology and Bioengineering, vol. 44, no. 5, pp. 586–594, 1994. View at Publisher · View at Google Scholar · View at Scopus
  32. M. S. Graboski, “The production of synthesis gas from methane, coal and biomass,” in Catalytic Conversion of Synthesis Gas and Alcohols to Chemicals, R. G. Herman, Ed., pp. 37–52, Plenum Press, New York, NY, USA, 1984. View at Google Scholar
  33. J. Sipma, A. M. Henstra, S. M. Parshina, P. N. Lens, G. Lettinga, and A. J. Stams, “Microbial CO conversions with applications in synthesis gas purification and bio-desulfurization,” Critical Reviews in Biotechnology, vol. 26, no. 1, pp. 41–65, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. G. Mörsdorf, K. Frunzke, D. Gadkari, and O. Meyer, “Microbial growth on carbon monoxide,” Biodegradation, vol. 3, no. 1, pp. 61–82, 1992. View at Publisher · View at Google Scholar · View at Scopus
  35. M. N. Davidova, N. B. Tarasova, F. K. Mukhitova, and I. U. Karpilova, “Carbon monoxide in metabolism of anaerobic bacteria,” Canadian Journal of Microbiology, vol. 40, no. 6, pp. 417–425, 1994. View at Google Scholar · View at Scopus
  36. T. G. Sokolova, A. M. Henstra, J. Sipma, S. N. Parshina, A. J. M. Stams, and A. V. Lebedinsky, “Diversity and ecophysiological features of thermophilic carboxydotrophic anaerobes,” FEMS Microbiology Ecology, vol. 68, no. 2, pp. 131–141, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. J. P. Amend and E. L. Shock, “Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria,” FEMS Microbiology Reviews, vol. 25, no. 2, pp. 175–243, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. F. S. Lupton, R. Conrad, and J. G. Zeikus, “CO metabolism of Desulfovibrio vulgaris strain Madison: physiological function in the absence or presence of exogeneous substrates,” FEMS Microbiology Letters, vol. 23, no. 2-3, pp. 263–268, 1984. View at Google Scholar · View at Scopus
  39. K. Jansen, R. K. Thauer, F. Widdel, and G. Fuchs, “Carbon assimilation pathways in sulfate reducing bacteria. Formate, carbon dioxide, carbon monoxide, and acetate assimilation by Desulfovibrio baarsii,” Archives of Microbiology, vol. 138, no. 3, pp. 257–262, 1984. View at Google Scholar · View at Scopus
  40. I. I. Karpilova, M. N. Davydova, and M. I. Beliaeva, “The effect of carbon monoxide on the growth of sulfate-reducing bacteria and their oxidation of this substrate,” Nauchnye Doklady Vysshei Shkoly. Biologicheskie Nauki, no. 1, pp. 85–88, 1983 (Russian). View at Google Scholar
  41. C. M. Plugge, M. Balk, and A. J. M. Stams, “Desulfotomaculum thermobenzoicum subsp. thermosyntrophicum subsp. nov., a thermophilic, syntrophic, propionate-oxidizing, spore-forming bacterium,” International Journal of Systematic and Evolutionary Microbiology, vol. 52, no. 2, pp. 391–399, 2002. View at Google Scholar · View at Scopus
  42. K. O. Stetter, G. Laurer, M. Thomm, and A. Neuner, “Isolation of extremely thermophilic sulfate reducers: evidence for a novel branch of archaebacteria,” Science, vol. 236, no. 4803, pp. 822–824, 1987. View at Google Scholar · View at Scopus
  43. K. O. Stetter, “Archaeoglobus fulgidus gen. nov., sp. nov.: a new taxon of extremely thermophilic archaebacteria,” Systematic and Applied Microbiollogy, vol. 10, pp. 172–173, 1988. View at Google Scholar
  44. V. A. Svetlichny, T. G. Sokolova, M. Gerhardt, M. Ringpfeil, N. A. Kostrikina, and G. A. Zavarzin, “Carboxydothermus hydrogenoformans gen. nov., sp. nov., a CO-utilizing thermophilic anaerobic bacterium from hydrothermal environments of Kunashir Island,” Systematic and Applied Microbiology, vol. 14, no. 3, pp. 254–260, 1991. View at Google Scholar · View at Scopus
  45. L. L. Campbell and J. R. Postgate, “Classification of the sporeforming sulphate-reducing bacteria,” Bacteriology Reviews, vol. 29, pp. 359–363, 1965. View at Google Scholar
  46. J. Kuever and F. A. Rainey, “Genus Desulfotomaculum Campbell and Postgate 1965, 361AL,” in Bergey's Manual of Systematic Bacteriology, P. De Vos, G. M. Garrity, D. Jones, F. A. Reiney, K.-H. Schleifer, and W. B. Whitman, Eds., vol. 3, pp. 989–996, 2009. View at Google Scholar
  47. K. Mori, M. Hatsu, R. Kimura, and K. Takamizawa, “Effect of heavy metals on the growth of a methanogen in pure culture and coculture with a sulfate-reducing bacterium,” Journal of Bioscience and Bioengineering, vol. 90, no. 3, pp. 260–265, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. F. K. Mukhitova, I. N. Ryazantseva, I. I. Karpilova, and M. I. Belyaeva, “The utilization of carbon monoxide by bacteria of Desulfovibrio genus,” Izevestiya Akademii Nauk SSSR, no. 6, pp. 944–948, 1983 (Russian). View at Google Scholar
  49. L. A. du Preez, J. P. Odendaal, J. P. Maree, and M. Ponsonby, “Biological removal of sulphate from industrial effluents using producer gas as energy source,” Environmental Technology, vol. 13, no. 9, pp. 875–882, 1992. View at Google Scholar · View at Scopus
  50. L. A. du Preez and J. P. Maree, “Pilot-scale biological sulphate and nitrate removal utilizing producer gas as energy source,” Water Science and Technology, vol. 30, no. 12, pp. 275–285, 1994. View at Google Scholar · View at Scopus
  51. R. T. van Houten, H. van der Spoel, A. C. van Aelst, L. W. Hulshoff Pol, and G. Lettinga, “Biological sulfate reduction using synthesis gas as energy and carbon source,” Biotechnology and Bioengineering, vol. 50, no. 2, pp. 136–144, 1996. View at Publisher · View at Google Scholar · View at Scopus
  52. A. M. Henstra, J. Sipma, A. Rinzema, and A. J. Stams, “Microbiology of synthesis gas fermentation for biofuel production,” Current Opinion in Biotechnology, vol. 18, no. 3, pp. 200–206, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. R. H. Perry, D. W. Green, and J. O. Maloney, Perry's Chemical Engineers' Handbook, Graw-Hill, New York, NY, USA, 1997.
  54. R. T. van Houten, Biological sulphate reduction with synthesis gas, Ph.D. thesis, Wageningen Academic Publishers, Wageningen, The Netherlands, 1996.
  55. R. T. van Houten and G. Lettinga, “Biological sulphate reduction with synthesis gas: microbiology and technology,” in Progress in Biotechnology, R. H. Wijffels, R. M. Buitelaar, C. Bucke, and J. Tramper, Eds., pp. 793–799, Elsevier, Amsterdam, The Netherlands, 1996. View at Google Scholar
  56. J. Sipma, M. B. Osuna, S. N. Parshina, G. Lettinga, A. J. M. Stams, and P. N. L. Lens, “H2 enrichment from synthesis gas by Desulfotomaculum carboxydivorans for potential applications in synthesis gas purification and biodesulfurization,” Applied Microbiology and Biotechnology, vol. 76, no. 2, pp. 339–347, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. H. Min and S. H. Zinder, “Isolation and characterization of a thermophilic sulfate-reducing bacterium Desulfotomaculum thermoacetoxidans sp. nov.,” Archives of Microbiology, vol. 153, no. 4, pp. 399–404, 1990. View at Google Scholar · View at Scopus
  58. E. A. Henry, R. Devereux, J. S. Maki et al., “Characterization of a new thermophilic sulfate-reducing bacterium. Thermodesulfovibrio yellowstonii, gen. nov. and sp. nov.: its phylogenetic relationship to Thermodesulfobacterium commune and their origins deep within the bacterial domain,” Archives of Microbiology, vol. 161, no. 1, pp. 62–69, 1994. View at Publisher · View at Google Scholar · View at Scopus
  59. G. P. Roberts, H. Youn, and R. L. Kerby, “CO-Sensing mechanisms,” Microbiology and Molecular Biology Reviews, vol. 68, no. 3, pp. 453–473, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. G. M. King and C. F. Weber, “Distribution, diversity and ecology of aerobic CO-oxidizing bacteria,” Nature Reviews Microbiology, vol. 5, no. 2, pp. 107–118, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. E. Oelgeschläger and M. Rother, “Carbon monoxide-dependent energy metabolism in anaerobic bacteria and archaea,” Archives of Microbiology, vol. 190, no. 3, pp. 257–269, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. J. M. Odom and H. D. Peck Jr., “Hydrogen cycling as a general mechanism for energy coupling in the sulfate-reducing bacteria. Desulfovibrio sp,” FEMS Microbiology Letters, vol. 12, no. 1, pp. 47–50, 1981. View at Publisher · View at Google Scholar · View at Scopus
  63. J. F. Heidelberg, R. Seshadri, S. A. Haveman et al., “The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough,” Nature Biotechnology, vol. 22, no. 5, pp. 554–559, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. A. J. Pierik, M. Hulstein, W. R. Hagen, and S. P. J. Albracht, “A low-spin iron with CN and CO as intrinsic ligands forms the core of the active site in [Fe]-hydrogenases,” European Journal of Biochemistry, vol. 258, no. 2, pp. 572–578, 1998. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Nicolet, C. Piras, P. Legrand, C. E. Hatchikian, and J. C. Fontecilla-Camps, “Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center,” Structure, vol. 7, no. 1, pp. 13–23, 1999. View at Publisher · View at Google Scholar · View at Scopus
  66. B. J. Lemon and J. W. Peters, “Iron-only hydrogenases,” in Handbook of Metalloproteins, A. Messerschmidt, R. Huber, T. Poulus, and K. Wieghardt, Eds., pp. 738–751, Wiley, New York, NY, USA, 2001. View at Google Scholar
  67. C. Greco, M. Bruschi, J. Heimdal, P. Fantucci, L. de Gioia, and U. Ryde, “Structural insights into the active-ready form of [FeFe]-hydrogenase and mechanistic details of its inhibition by carbon monoxide,” Inorganic Chemistry, vol. 46, no. 18, pp. 7256–7258, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Y. Mityashina and M. N. Davydova, “Effects of carbon monoxide on the nucleotide content of Desulfovibrio desulfuricans B-1388,” Applied Biochemistry and Microbiology, vol. 31, pp. 547–549, 1995. View at Google Scholar
  69. S. Y. Mityashina and M. N. Davydova, “Characteristics of the energy state of Desulfovibrio desulfuricans B-1388 cells growing in lactate-sulfate medium under an atmosphere of argon plus carbon monoxide,” Microbiology, vol. 67, pp. 471–475, 1998 (Russian). View at Google Scholar
  70. M. Davydova, R. Sabirova, N. Vylegzhanina, and N. Tarasova, “Carbon monoxide and oxidative stress in Desulfovibrio desulfuricans B-1388,” Journal of Biochemical and Molecular Toxicology, vol. 18, no. 2, pp. 87–91, 2004. View at Publisher · View at Google Scholar · View at Scopus
  71. B. J. Lemon and J. W. Peters, “Binding of exogenously added carbon monoxide at the active site of the iron-only hydrogenase (CpI) from Clostridium pasteurianum,” Biochemistry, vol. 38, no. 40, pp. 12969–12973, 1999. View at Publisher · View at Google Scholar · View at Scopus
  72. P. P. Liebgott, F. Leroux, B. Burlat et al., “Relating diffusion along the substrate tunnel and oxygen sensitivity in hydrogenase,” Nature Chemical Biology, vol. 6, no. 1, pp. 63–70, 2010. View at Google Scholar · View at Scopus
  73. D. Chivian, E. L. Brodie, E. J. Alm et al., “Environmental genomics reveals a single-species ecosystem deep within earth,” Science, vol. 322, no. 5899, pp. 275–278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. D. Shelver, R. L. Kerby, Y. He, and G. P. Roberts, “CooA, a CO-sensing transcription factor from Rhodospirillum rubrum, is a CO-binding heme protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 21, pp. 11216–11220, 1997. View at Publisher · View at Google Scholar · View at Scopus
  75. J. D. Fox, R. L. Kerby, G. P. Roberts, and P. W. Ludden, “Characterization of the CO-induced, CO-tolerant hydrogenase from Rhodospirillum rubrum and the gene encoding the large subunit of the enzyme,” Journal of Bacteriology, vol. 178, no. 6, pp. 1515–1524, 1996. View at Google Scholar · View at Scopus
  76. R. L. Kerby, P. W. Ludden, and G. P. Roberts, “Carbon monoxide-dependent growth of Rhodospirillum rubrum,” Journal of Bacteriology, vol. 177, no. 8, pp. 2241–2244, 1995. View at Google Scholar · View at Scopus
  77. G. Voordouw, “Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough,” Journal of Bacteriology, vol. 184, no. 21, pp. 5903–5911, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. N. B. Tarasova and M. I. Belyaeva, “The CO dehydrogenase activity of Desulfovibrio desulfuricans growing under chemoorganotrophic and chemolithoheterotrophic conditions,” Microbiology, vol. 67, no. 5, pp. 504–508, 1998. View at Google Scholar · View at Scopus
  79. J. Sipma, P. N. L. Lens, A. J. M. Stams, and G. Lettinga, “Carbon monoxide conversion by anaerobic bioreactor sludges,” FEMS Microbiology Ecology, vol. 44, no. 2, pp. 271–277, 2003. View at Publisher · View at Google Scholar · View at Scopus
  80. J. Sipma, G. Lettinga, A. J. M. Stams, and P. N. L. Lens, “Hydrogenogenic CO conversion in a moderately thermophilic (55°C) sulfate-fed gas lift reactor: competition for CO-derived H2,” Biotechnology Progress, vol. 22, no. 5, pp. 1327–1334, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Sipma, Microbial hydrogenotrophic CO conversions: applications in synthesis gas purification and biodesulfurization, Ph.D. thesis, Wageningen University, Wageningen, The Netherlands, 2006.
  82. J. Sipma, M. B. Osuna, G. Lettinga, A. J. M. Stams, and P. N. L. Lens, “Effect of hydraulic retention time on sulfate reduction in a carbon monoxide fed thermophilic gas lift reactor,” Water Research, vol. 41, no. 9, pp. 1995–2003, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. M. V. G. Vallero, R. H. M. Treviño, P. L. Paulo, G. Lettinga, and P. N. L. Lens, “Effect of sulfate on methanol degradation in thermophilic (55°C) methanogenic UASB reactors,” Enzyme and Microbial Technology, vol. 32, no. 6, pp. 676–687, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. R. T. van Houten, S. Y. Yun, and G. Lettinga, “Thermophilic sulphate and sulphite reduction in lab-scale gas-lift reactors using H2 and CO2 as energy and carbon source,” Biotechnology and Bioengineering, vol. 55, no. 5, pp. 807–814, 1997. View at Google Scholar · View at Scopus
  85. J. C. M. Scholten, R. Conrad, and A. J. M. Stams, “Effect of 2-bromo-ethane sulfonate, molybdate and chloroform on acetate consumption by methanogenic and sulfate-reducing populations in freshwater sediment,” FEMS Microbiology Ecology, vol. 32, no. 1, pp. 35–42, 2000. View at Publisher · View at Google Scholar · View at Scopus
  86. J. Sipma, R. J. W. Meulepas, S. N. Parshina, A. J. M. Stams, G. Lettinga, and P. N. L. Lens, “Effect of carbon monoxide, hydrogen and sulfate on thermophilic (55°C) hydrogenogenic carbon monoxide conversion in two anaerobic bioreactor sludges,” Applied Microbiology and Biotechnology, vol. 64, no. 3, pp. 421–428, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. S.-E. Oh, S. van Ginkel, and B. E. Logan, “The relative effectiveness of pH control and heat treatment for enhancing biohydrogen gas production,” Environmental Science and Technology, vol. 37, no. 22, pp. 5186–5190, 2003. View at Publisher · View at Google Scholar · View at Scopus
  88. C.-C. Chen, C.-Y. Lin, and M.-C. Lin, “Acid-base enrichment enhances anaerobic hydrogen production process,” Applied Microbiology and Biotechnology, vol. 58, no. 2, pp. 224–228, 2002. View at Publisher · View at Google Scholar · View at Scopus
  89. J. Weijma, E. A. A. Bots, G. Tandlinger, A. J. M. Stams, L. W. Hulshoff Pol, and G. Lettinga, “Optimisation of sulphate reduction in a methanol-fed thermophilic bioreactor,” Water Research, vol. 36, no. 7, pp. 1825–1833, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. R. Sparling, D. Risbey, and H. M. Poggi-Varaldo, “Hydrogen production from inhibited anaerobic composters,” International Journal of Hydrogen Energy, vol. 22, no. 6, pp. 563–566, 1997. View at Google Scholar · View at Scopus
  91. A. de Smul and W. Verstraete, “The phenomenology and the mathematical modeling of the silicone-supported chemical oxidation of aqueous sulfide to elemental sulfur by ferric sulphate,” Journal of Chemical Technology and Biotechnology, vol. 74, no. 5, pp. 456–466, 1999. View at Google Scholar · View at Scopus
  92. R. Cord-Ruwisch, H.-J. Seitz, and R. Conrad, “The capacity of hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen depends on the redox potential of the terminal electron acceptor,” Archives of Microbiology, vol. 149, no. 4, pp. 350–357, 1988. View at Publisher · View at Google Scholar · View at Scopus