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Volume 2015, Article ID 235384, 12 pages
http://dx.doi.org/10.1155/2015/235384
Research Article

Assessment of the Carbon Monoxide Metabolism of the Hyperthermophilic Sulfate-Reducing Archaeon Archaeoglobus fulgidus VC-16 by Comparative Transcriptome Analyses

Department of Biology, Centre for Geobiology, University of Bergen, 5020 Bergen, Norway

Received 10 April 2015; Revised 9 June 2015; Accepted 14 June 2015

Academic Editor: Uwe Deppenmeier

Copyright © 2015 William P. Hocking 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. S. M. Techtmann, A. S. Colman, and F. T. Robb, “‘That which does not kill us only makes us stronger’: the role of carbon monoxide in thermophilic microbial consortia: minireview,” Environmental Microbiology, vol. 11, no. 5, pp. 1027–1037, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. A. M. Henstra, C. Dijkema, and A. J. M. Stams, “Archaeoglobus fulgidus couples CO oxidation to sulfate reduction and acetogenesis with transient formate accumulation,” Environmental Microbiology, vol. 9, no. 7, pp. 1836–1841, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. S. N. Parshina, J. Sipma, A. M. Henstra, and A. J. M. Stams, “Carbon monoxide as an electron donor for the biological reduction of sulphate,” International Journal of Microbiology, vol. 2010, Article ID 319527, 9 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. 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 Publisher · View at Google Scholar · View at Scopus
  5. R. Rabus, T. Hansen, and F. Widdel, “Dissimilatory sulfate- and sulfur-reducing prokaryotes,” in The Prokaryotes Volume 2: Ecophysiology and Biochemistry, M. Dworkin, S. Falkow, E. Rosenberg, K. Schleifer, and E. Stackebrandt, Eds., pp. 659–768, Springer, 2006. View at Google Scholar
  6. N. Khelifi, V. Grossi, M. Hamdi et al., “Anaerobic oxidation of fatty acids and alkenes by the hyperthermophilic sulfate-reducing archaeon Archaeoglobus fulgidus,” Applied and Environmental Microbiology, vol. 76, no. 9, pp. 3057–3060, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Parthasarathy, J. Kahnt, N. P. Chowdhury, and W. Buckel, “Phenylalanine catabolism in Archaeoglobus fulgidus VC-16,” Archives of Microbiology, vol. 195, no. 12, pp. 791–797, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Sokolova and A. Lebedinsky, “CO-oxidizing anaerobic thermophilic prokaryotes,” in Thermophilic Microbes in Environmental and Industrial Biotechnology, T. Satyanarayana, J. Littlechild, and Y. Kawarabayasi, Eds., pp. 203–228, Springer, Dordrecht, The Netherlands, 2013. View at Google Scholar
  9. H.-P. Klenk, R. A. Clayton, J.-F. Tomb et al., “The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus,” Nature, vol. 390, no. 6658, pp. 364–370, 1997. View at Publisher · View at Google Scholar · View at Scopus
  10. Y.-R. Dai, D. W. Reed, J. H. Millstein, P. L. Hartzell, D. A. Grahame, and E. DeMoll, “Acetyl-CoA decarbonylase/synthase complex from Archaeoglobus fulgidus,” Archives of Microbiology, vol. 169, no. 6, pp. 525–529, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. S. M. Techtmann, A. V. Lebedinsky, A. S. Colman et al., “Evidence for horizontal gene transfer of anaerobic carbon monoxide dehydrogenases,” Frontiers in Microbiology, vol. 3, article 132, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Möller-Zinkhan and R. K. Thauer, “Anaerobic lactate oxidation to 3 CO2 by Archaeoglobus fulgidus via the carbon monoxide dehydrogenase pathway: demonstration of the acetyl-CoA carbon-carbon cleavage reaction in cell extracts,” Archives of Microbiology, vol. 153, no. 3, pp. 215–218, 1990. View at Publisher · View at Google Scholar · View at Scopus
  13. W. P. Hocking, R. Stokke, I. Roalkvam, and I. H. Steen, “Identification of key components in the energy metabolism of the hyperthermophilic sulfate-reducing archaeon Archaeoglobus fulgidus by transcriptome analyses,” Frontiers in Microbiology, vol. 5, article 95, Article ID Article 95, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. 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
  15. 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
  16. B. J. Tindall, K. O. Stetter, and M. D. Collins, “A novel, fully saturated menaquinone from the thermophilic, sulphate-reducing archaebacterium Archaeoglobus fulgidus,” Journal of General Microbiology, vol. 135, pp. 693–696, 1989. View at Google Scholar
  17. J. Kunow, B. Schwörer, K. O. Stetter, and R. K. Thauer, “A F420-dependent NADP reductase in the extremely thermophilic sulfate-reducing Archaeoglobus fulgidus,” Archives of Microbiology, vol. 160, no. 3, pp. 199–205, 1993. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Brüggemann, F. Falinski, and U. Deppenmeier, “Structure of the F420H2:quinone oxidoreductase of Archaeoglobus fulgidus,” European Journal of Biochemistry, vol. 267, no. 18, pp. 5810–5814, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. R. K. Thauer, E. Stackebrandt, and W. A. Hamilton, “Energy metabolism phylogenetic diversity of sulphate-reducing bacteria,” in Sulphate-Reducing Bacteria, L. L. Barton and and W. A. Hamilton, Eds., pp. 1–38, 2007. View at Google Scholar
  20. G. J. Mander, E. C. Duin, D. Linder, K. O. Stetter, and R. Hedderich, “Purification and characterization of a membrane-bound enzyme complex from the sulfate-reducing archaeon Archaeoglobus fulgidus related to heterodisulfide reductase from methanogenic archaea,” European Journal of Biochemistry, vol. 269, no. 7, pp. 1895–1904, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. I. A. C. Pereira, A. R. Ramos, F. Grein, M. C. Marques, S. M. da Silva, and S. S. Venceslau, “A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and archaea,” Frontiers in Microbiology, vol. 2, article 69, 2011. View at Publisher · View at Google Scholar
  22. F. Grein, A. R. Ramos, S. S. Venceslau, and I. A. C. Pereira, “Unifying concepts in anaerobic respiration: insights from dissimilatory sulfur metabolism,” Biochimica et Biophysica Acta, vol. 1827, no. 2, pp. 145–160, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. A. R. Ramos, K. L. Keller, J. D. Wall, and I. A. C. Pereira, “The membrane qmoABC complex interacts directly with the dissimilatory adenosine 5′-phosphosulfate reductase in sulfate reducing bacteria,” Frontiers in Microbiology, vol. 3, Article ID Article 137, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Burggraf, H. W. Jannasch, B. Nicolaus, and K. O. Stetter, “Archaeoglobus profundus sp. nov., represents a new species within the sulfate-reducing archaebacteria,” Systematic and Applied Microbiology, vol. 13, no. 1, pp. 24–28, 1990. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Huber, H. Jannasch, R. Rachel, T. Fuchs, and K. O. Stetter, “Archaeoglobus veneficus sp. nov., a novel facultative chemolithoautotrophic hyperthermophilic sulfite reducer, isolated from abyssal black smokers,” Systematic and Applied Microbiology, vol. 20, no. 3, pp. 374–380, 1997. View at Publisher · View at Google Scholar · View at Scopus
  26. B. O. Steinsbu, I. H. Thorseth, S. Nakagawa et al., “Archaeoglobus sulfaticallidus sp. nov., a thermophilic and facultatively lithoautotrophic sulfate-reducer isolated from black rust exposed to hot ridge flank crustal fluids,” International Journal of Systematic and Evolutionary Microbiology, vol. 60, no. 12, pp. 2745–2752, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. L. M. Siegel, “A direct microdetermination for sulfide,” Analytical Biochemistry, vol. 11, no. 1, pp. 126–132, 1965. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Cord-Ruwisch, “A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria,” Journal of Microbiological Methods, vol. 4, no. 1, pp. 33–36, 1985. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Fellenberg, N. C. Hauser, B. Brors, A. Neutzner, J. D. Hoheisel, and M. Vingron, “Correspondence analysis applied to microarray data,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 19, pp. 10781–10786, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. I. Wolf, K. S. Makarova, N. Yutin, and E. V. Koonin, “Updated clusters of orthologous genes for Archaea: a complex ancestor of the Archaea and the byways of horizontal gene transfer,” Biology Direct, vol. 7, no. 1, article 46, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. T. H. C. Brondijk, A. Nilavongse, N. Filenko, D. J. Richardson, and J. A. Cole, “NapGH components of the periplasmic nitrate reductase of Escherichia coli K-12: Location, topology and physiological roles in quinol oxidation and redox balancing,” Biochemical Journal, vol. 379, no. 1, pp. 47–55, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. I. Anderson, C. Risso, D. Holmes et al., “Complete genome sequence of Ferroglobus placidus AEDII12DO,” Standards in Genomic Sciences, vol. 5, no. 1, pp. 50–60, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. W. Zhang, D. E. Culley, J. C. M. Scholten, M. Hogan, L. Vitiritti, and F. J. Brockman, “Global transcriptomic analysis of Desulfovibrio vulgaris on different electron donors,” Antonie van Leeuwenhoek, vol. 89, no. 2, pp. 221–237, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Fiévet, L. My, E. Cascales et al., “The anaerobe-specific orange protein complex of Desulfovibrio vulgaris hildenborough is encoded by two divergent operons coregulated by σ54 and a cognate transcriptional regulator,” Journal of Bacteriology, vol. 193, no. 13, pp. 3207–3219, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. L. Pieulle, P. Stocker, M. Vinay et al., “Study of the thiol/disulfide redox systems of the anaerobe Desulfovibrio vulgaris points out pyruvate:ferredoxin oxidoreductase as a new target for thioredoxin,” Journal of Biological Chemistry, vol. 286, no. 10, pp. 7812–7821, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. P. M. Pereira, Q. He, F. M. A. Valente et al., “Energy metabolism in Desulfovibrio vulgaris Hildenborough: insights from transcriptome analysis,” Antonie van Leeuwenhoek, vol. 93, no. 4, pp. 347–362, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. K. L. Tkaczuk, S. Dunin-Horkawicz, E. Purta, and J. M. Bujnicki, “Structural and evolutionary bioinformatics of the SPOUT superfamily of methyltransferases,” BMC Bioinformatics, vol. 8, article 73, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Rother, E. Oelgeschläger, and W. W. Metcalf, “Genetic and proteomic analyses of CO utilization by Methanosarcina acetivorans,” Archives of Microbiology, vol. 188, no. 5, pp. 463–472, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. N. Matschiavelli, E. Oelgeschläger, B. Cocchiararo, J. Finke, and M. Rother, “Function and regulation of isoforms of carbon monoxide dehydrogenase/acetyl coenzyme A synthase in Methanosarcina acetivorans,” Journal of Bacteriology, vol. 194, no. 19, pp. 5377–5387, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Simon and M. Kern, “Quinone-reactive proteins devoid of haem b form widespread membrane-bound electron transport modules in bacterial respiration,” Biochemical Society Transactions, vol. 36, no. 5, pp. 1011–1016, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Simon and M. G. Klotz, “Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations,” Biochimica et Biophysica Acta, vol. 1827, no. 2, pp. 114–135, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Kern and J. Simon, “Characterization of the NapGH quinol dehydrogenase complex involved in Wolinella succinogenes nitrate respiration,” Molecular Microbiology, vol. 69, no. 5, pp. 1137–1152, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Rother and W. W. Metcalf, “Anaerobic growth of Methanosarcina acetivorans C2A on carbon monoxide: an unusual way of life for a methanogenic archaeon,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 48, pp. 16929–16934, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. D. J. Lessner, L. Li, Q. Li et al., “An unconventional pathway for reduction of CO2 to methane in CO-grown Methanosarcina acetivorans revealed by proteomics,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 47, pp. 17921–17926, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. G. J. Mander, M. S. Weiss, R. Hedderich, J. Kahnt, U. Ermler, and E. Warkentin, “X-ray structure of the γ-subunit of a dissimilatory sulfite reductase: fixed and flexible C-terminal arms,” FEBS Letters, vol. 579, no. 21, pp. 4600–4604, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. T. F. Oliveira, C. Vonrhein, P. M. Matias, S. S. Venceslau, I. A. C. Pereira, and M. Archer, “The crystal structure of Desulfovibrio vulgaris dissimilatory sulfite reductase bound to DsrC provides novel insights into the mechanism of sulfate respiration,” The Journal of Biological Chemistry, vol. 283, no. 49, pp. 34141–34149, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Bäumer, T. Ide, C. Jacobi, A. Johann, G. Gottschalk, and U. Deppenmeier, “The F420H2 dehydrogenase from Methanosarcina mazei is a redox-driven proton pump closely related to NADH dehydrogenases,” The Journal of Biological Chemistry, vol. 275, no. 24, pp. 17968–17973, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. Y.-J. Moon, J. Kwon, S.-H. Yun et al., “Proteome analyses of hydrogen-producing hyperthermophilic archaeon Thermococcus onnurineus NA1 in different one-carbon substrate culture conditions.,” Molecular & cellular proteomics : MCP, vol. 11, no. 6, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Vornolt, J. Kunow, K. O. Stetter, and R. K. Thauer, “Enzymes and coenzymes of the carbon monoxide dehydrogenase pathway for autotrophic CO2 fixation in Archaeoglobus lithotrophicus and the lack of carbon monoxide dehydrogenase in the heterotrophic A. profundus,” Archives of Microbiology, vol. 163, no. 2, pp. 112–118, 1995. View at Publisher · View at Google Scholar · View at Scopus
  50. C. Welte and U. Deppenmeier, “Re-evaluation of the function of the F420 dehydrogenase in electron transport of Methanosarcina mazei,” The FEBS Journal, vol. 278, no. 8, pp. 1277–1287, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Welte and U. Deppenmeier, “Membrane-bound electron transport in Methanosaeta thermophila,” Journal of Bacteriology, vol. 193, no. 11, pp. 2868–2870, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. G. J. Mander, A. J. Pierik, H. Huber, and R. Hedderich, “Two distinct heterodisulfide reductase-like enzymes in the sulfate-reducing archaeon Archaeoglobus profundus,” European Journal of Biochemistry, vol. 271, no. 6, pp. 1106–1116, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. 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, Article ID 63780, pp. 2159–2165, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. R. L. Kerby, S. S. Hong, S. A. Ensign, L. J. Coppoc, P. W. Ludden, and G. P. Roberts, “Genetic and physiological characterization of the Rhodospirillum rubrum carbon monoxide dehydrogenase system,” Journal of Bacteriology, vol. 174, no. 16, pp. 5284–5294, 1992. View at Google Scholar · View at Scopus
  55. S. W. M. Kengen, J. van der Oost, and W. M. De Vos, “Molecular characterization of H2O2-forming NADH oxidases from Archaeoglobus fulgidus,” European Journal of Biochemistry, vol. 270, no. 13, pp. 2885–2894, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. M. von Jan, A. Lapidus, T. G. Del Rio et al., “Complete genome sequence of Archaeoglobus profundus type strain (AV18),” Standards in Genomic Sciences, vol. 2, no. 3, pp. 327–346, 2010. View at Publisher · View at Google Scholar · View at Scopus