Journal of Bioenergetics and Biomembranes

, Volume 36, Issue 1, pp 77–91 | Cite as

Dissimilatory Oxidation and Reduction of Elemental Sulfur in Thermophilic Archaea

  • Arnulf Kletzin
  • Tim Urich
  • Fabian Müller
  • Tiago M. Bandeiras
  • Cláudio M. Gomes


The oxidation and reduction of elemental sulfur and reduced inorganic sulfur species are some of the most important energy-yielding reactions for microorganisms living in volcanic hot springs, solfataras, and submarine hydrothermal vents, including both heterotrophic, mixotrophic, and chemolithoautotrophic, carbon dioxide-fixing species. Elemental sulfur is the electron donor in aerobic archaea like Acidianus and Sulfolobus. It is oxidized via sulfite and thiosulfate in a pathway involving both soluble and membrane-bound enzymes. This pathway was recently found to be coupled to the aerobic respiratory chain, eliciting a link between sulfur oxidation and oxygen reduction at the level of the respiratory heme copper oxidase. In contrast, elemental sulfur is the electron acceptor in a short electron transport chain consisting of a membrane-bound hydrogenase and a sulfur reductase in (facultatively) anaerobic chemolithotrophic archaea Acidianus and Pyrodictium species. It is also the electron acceptor in organoheterotrophic anaerobic species like Pyrococcus and Thermococcus, however, an electron transport chain has not been described as yet. The current knowledge on the composition and properties of the aerobic and anaerobic pathways of dissimilatory elemental sulfur metabolism in thermophilic archaea is summarized in this contribution.

Sulfur oxygenase reductase thiosulfate:quinone oxidoreductase sulfite:acceptor oxidoreductase heme copper oxidase sulfur reductase hydrogenase Rieske ferredoxin Acidianus Pyrodictium Pyrococcus 


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  1. Aagaard, A., Gilderson, G., Gomes, C. M., Teixeira, M., and Brzezinski, P. (1999). Biochemistry. 38, 10032-10041.Google Scholar
  2. Adams, M. W., Holden, J. F., Menon, A. L., Schut, G. J., Grunden, A. M., Hou, C., Hutchins, A. M., Jenney, F. E., Jr., Kim, C., Ma, K., Pan, G., Roy, R., Sapra, R., Story, S. V., and Verhagen, M. F. (2001). J. Bacteriol. 183 Google Scholar
  3. Amend, J. P., and Shock, E. L. (2001). FEMS Microbiol. Rev. 25, 175-243.Google Scholar
  4. Arendsen, A. F., Veenhuizen, P. T., and Hagen, W. R. (1995). FEBS Lett. 368, 117-121.Google Scholar
  5. Bandeiras, T. M., Salgueiro, C., Kletzin, A., Gomes, C. M., Teixeira, M. (2002). FEBS Lett. 531, 273-277.Google Scholar
  6. Barns, S. M., Fundya, R. E., Jeffries, M. W., and Pace, N. R. (1994). Proc. Natl. Acad. Sci. 91, 1609-1613.Google Scholar
  7. Blamey, J. M., and Adams, M. W. W. (1993). Biochim. Biophys. Acta 1161, 19-27.Google Scholar
  8. Blöchl, E., Burggraf, S., Fiala, F., Lauerer, G., Huber, G., Huber, R., Rachel, R., Segerer, A., Stetter, K. O., and Völkl, P. (1995). World J. Microbiol. Biotechnol. 11, 9-16.Google Scholar
  9. Brierley, C. L., and Brierley, J. A. (1973). Can. J. Microbiol. 19, 183-188.Google Scholar
  10. Brierley, C. L., and Brierley, J. A. (1982). Zbl. Bakt. Hyg., I. Abt. Orig. C 3, 289-294.Google Scholar
  11. Brock, T. D., Brock, K. M., Belly, R. T., and Weiss, R. L. (1972). Arch. Microbiol. 84, 54-68.Google Scholar
  12. Brüser, T., Selmer, T., and Dahl, C. (2000). J. Biol. Chem. 275, 1691-1698.Google Scholar
  13. Bryant, F. O., and Adams, M. W. (1989). J. Biol. Chem. 264, 5070-5079.Google Scholar
  14. Dahl, C., Molitor, M., and Trüper, H. G. (2001). Methods Enzymol. 331, 410-419.Google Scholar
  15. Dahl, C., and Trüper, H. G. (2001). Methods Enzymol. 331, 427-441.Google Scholar
  16. Daniels, L., Belay, N., and Rajagopal, B. S. (1986). Appl. Environ. Microbiol. 51, 703-709.Google Scholar
  17. Das, T. K., Gomes, C. M., Teixeira, M., and Rousseau, D. L. (1999). Proc. Natl. Acad. Sci. U.S.A. 96, 9591-9596Google Scholar
  18. Dietrich, W., and Klimmek, O. (2002). Eur. J. Biochem. 269, 1086-1095.Google Scholar
  19. Dirmeier, R., Keller, M., Frey, G., Huber, H., and Stetter, K. O. (1998). Eur. J. Biochem. 252, 486-491.Google Scholar
  20. Emmel, T., Sand, W., König, W. A., and Bock, E. (1986). J. Gen. Microbiol. 132, 3415-3420.Google Scholar
  21. Fischer, F., Zillig, W., Stetter, K. O., and Schreiber, G. (1983). Nature 301, 511-513.Google Scholar
  22. Friedrich, C. G. (1998). Adv. Microb. Physiol. 39, 235-289.Google Scholar
  23. Friedrich, C. G., Rother, D., Bardischewsky, F., Quentmeier, A., and Fischer, J. (2001). Appl. Environ. Microbiol. 67, 2873-2882.Google Scholar
  24. Fritz, G., Roth, A., Schiffer, A., Buchert, T., Bourenkov, G., Bartunik, H. D., Huber, H., Stetter, K. O., Kroneck, P. M., and Ermler, U. (2002). Proc. Natl. Acad. Sci. U.S.A. 99, 1836-1841.Google Scholar
  25. Fuchs, T., Huber, H., Burggraf, S., and Stetter, K. O. (1996). Syst. Appl. Microbiol. 19, 56-60.Google Scholar
  26. Gomes, C. M. (1999). In Instituto Tecnologia Química e Biológica, PhD Thesis, Universidade Nova de Lisboa, Oeiras.Google Scholar
  27. Gomes, C. M., Backgren, C., Teixeira, M., Puustinen, A., Verkhovskaya, M. L., Wikström, M., and Verkhovsky, M. I. (2001a). FEBS Lett. 497, 159-64.Google Scholar
  28. Gomes, C. M., Bandeiras, T. M., and Teixeira, M. (2001b). J. Bioenerg. Biomembr. 33, 1-8.Google Scholar
  29. Gomes, C. M., Lemos, R. S., Teixeira, M., Kletzin, A., Huber, H., Stetter, K. O., Schäfer, G., and Anemüller, S. (1999). Biochim. Biophys. Acta 1411, 134-141.Google Scholar
  30. Griesbeck, C., Schutz, M., Schodl, T., Bathe, S., Nausch, L., Mederer, N., Vielreicher, M., and Hauska, G. (2002). Biochemistry 41, 11552-11565.Google Scholar
  31. Grogan, D. W. (1989). J. Bacteriol. 171, 6710-6719.Google Scholar
  32. He, Z., Li, Y., Zhou, P., and Liu, S. (2000). FEMS Microbiol. Lett. 193, 217-221.Google Scholar
  33. Hedderich, R., Klimmek, O., Kröger, A., Dirmeier, R., Keller, M., and Stetter, K. O. (1999). FEMS Microbiol. Rev. 22, 353-381.Google Scholar
  34. Hellwig, P., Gomes, C. M., and Teixeira, M. (2003). Biochemistry 42, 6179-6184.Google Scholar
  35. Holden, J. F., Poole, F. L., Tollaksen, S. L., Giometti, C. S., Lim, H., Yates, J. R., and Adams, M. W. W. (2001). Comp. Funct. Genom. 2, 275-288.Google Scholar
  36. Holland, H. D. (2002). Geochim. Cosmochim. Acta 66, 3811-3826.Google Scholar
  37. Huber, G., Drobner, E., Huber, H., and Stetter, K. O. (1992). Syst. Appl. Microbiol. 15, 502-504.Google Scholar
  38. Huber, R., Kristiansson, J. K., and Stetter, K. O. (1987). Arch. Microbiol. 149, 95-101.Google Scholar
  39. Hugler, M., Huber, H., Stetter, K. O., and Fuchs, G. (2003). Arch. Microbiol. 179, 160-173.Google Scholar
  40. Ishii, M., Miyake, T., Satoh, T., Sugiyama, H., Oshima, Y., Kodama, T., and Igarashi, Y. (1996). Arch. Microbiol. 166, 368-371.Google Scholar
  41. Kanai, T., Ito, S., and Imanaka, T. (2003). J. Bacteriol. 185, 1705-1711.Google Scholar
  42. Kappler, U., and Dahl, C. (2001). FEMS Microbiol. Lett. 203, 1-9.Google Scholar
  43. Kelly, D. P. (1982). Philos. Trans. R. Soc., Lond. Ser. B 298, 499-528.Google Scholar
  44. Kelly, D. P. (1988). In The Nitrogen and Sulphur Cycles (Cole, J. A., and Ferguson, S. J., eds.), Cambridge University Press, Cambridge, pp. 65-98.Google Scholar
  45. Kelly, D. P., Shergill, J. K., Lu, W. P., and Wood, A. P. (1997). Antonie Van Leeuwenhoek 71, 95-107.Google Scholar
  46. Kelly, D. P., and Wood, A. P. (1994). Methods Enzymol. 243, 501-510.Google Scholar
  47. Kengen, S. W. M., and Stams, A. J. M. (1994). FEMS Microbiol. Lett. 117, 305-309.Google Scholar
  48. Kisker, C., Schindelin, H., Pacheco, A., Wehbi, W. A., Garrett, R. M., Rajagopalan, K. V., and Enemark, J. H. D. C. (1997). Cell 91, 973-983.Google Scholar
  49. Kletzin, A. (1989). J. Bacteriol. 171, 1638-1643.Google Scholar
  50. Kletzin, A. (1992). J. Bacteriol. 174, 5854-5859.Google Scholar
  51. Kletzin, A. (1994). Syst. Appl. Microbiol. 16, 534-543.Google Scholar
  52. Larsson, L., Olsson, G., Holst, O., and Karlsson, H. T. (1990). Appl. Environ. Microbiol. 56, 697-701.Google Scholar
  53. Laska, S., and Kletzin, A. (2000). J. Chromatogr. B 737, 151-160.Google Scholar
  54. Laska, S., Lottspeich, F., and Kletzin, A. (2003). Microbiology 149, 2357-2371.Google Scholar
  55. Le Faou, A., Rajagopal, B. S., Daniels, L., and Fauque, G. (1990). FEMS Microbiol. Rev. 6, 351-381.Google Scholar
  56. Lemos, R. S., Gomes, C. M., and Teixeira, M. (2001). Biochem. Biophys. Res. Comm., 281, 141-150.Google Scholar
  57. Ma, K., and Adams, M. W. (1994). J. Bacteriol. 176, 6509-6517.Google Scholar
  58. Ma, K., and Adams, M. W. (2001). Methods Enzymol. 331, 208-216.Google Scholar
  59. Ma, K., Schicho, R. N., Kelly, R. M., and Adams, M. W. (1993). Proc. Natl. Acad. Sci. U.S.A. 90, 5341-5344.Google Scholar
  60. Ma, K., Weiss, R., and Adams, M. W. (2000). J. Bacteriol. 182, 1864-1871.Google Scholar
  61. Montegrossi, G., Tassi, F., Vaselli, O., Buccianti, A., and Garofalo, K. (2001). Anal. Chem., 73, 3709-3715.Google Scholar
  62. Mukund, S., and Adams, M. W. W. (1995). J. Biol. Chem. 270, 8389-8392.Google Scholar
  63. Nakamura, K., Nakamura, M., Yoshikawa, H., and Amano, Y. (2001). Biosci. Biotechnol. Biochem. 65, 102-108.Google Scholar
  64. Pihl, T. D., Black, L. K., Schulman, B. A., and Maier, R. J. (1992). J. Bacteriol. 174, 137-143.Google Scholar
  65. Pihl, T. D., and Maier, R. J. (1991). J. Bacteriol. 173, 1839-1844.Google Scholar
  66. Pihl, T. D., Schicho, R. N., Kelly, R. M., and Maier, R. J. (1989). Proc. Natl. Acad. Sci. U.S.A. 86, 138-141.Google Scholar
  67. Pley, U., Schipka, J., Gambacorta, A., Jannasch, H. W., Fricke, H., Rachel, R., and Stetter, K. O. (1991). Syst. Appl. Microbiol. 14, 245-253.Google Scholar
  68. Pronk, J. T., Meulenberg, R., Hazeu, W., Bos, P., and Kuenen, J. G. (1990). FEMS Microbiol. Rev. 75, 293-306.Google Scholar
  69. Purschke, W. G., Schmidt, C. L., Petersen, A., and Schäfer, G. (1997). J. Bacteriol. 179, 1344-1353.Google Scholar
  70. Quentmeier, A., and Friedrich, C. G. (2001). FEBS Lett. 503, 168-172.Google Scholar
  71. Reysenbach, A. L., Wickham, G. S., and Pace, N. R. (1994). Appl. Environ. Microbiol. 60, 2113-2119.Google Scholar
  72. Rother, D., Henrich, H. J., Quentmeier, A., Bardischewsky, F., and Friedrich, C. G. (2001). J. Bacteriol. 183, 4499-4508.Google Scholar
  73. Sapra, R., Bagramyan, K., and Adams, M. W. (2003). Proc. Natl. Acad. Sci. U.S.A. 100, 7545-7550.Google Scholar
  74. Sapra, R., Verhagen, M. F., and Adams, M. W. (2000). J. Bacteriol. 182, 3423-3428.Google Scholar
  75. Schäfer, A., Barkowski, C., and Fuchs, G. (1986). Arch. Microbiol. 146, 301-308.Google Scholar
  76. Schauder, R., and Kröger, A. (1993). Arch. Microbiol. 159, 491-497.Google Scholar
  77. Schicho, R. N., Ma, K., Adams, M. W., and Kelly, R. M. (1993). J. Bacteriol. 175, 1823-1830.Google Scholar
  78. Schönheit, P., and Schäfer, T. (1995). World J. Microbiol. Biotechnol. 11, 26-57.Google Scholar
  79. Schut, G., Zhou, J., and Adams, M. (2001). J. Bacteriol. 183, 7027-7036.Google Scholar
  80. Segerer, A., Stetter, K. O., and Klink, F. (1985). Nature 313, 787-789.Google Scholar
  81. Selig, M., and Schönheit, P. (1994). Arch. Microbiol. 162, 286-294.Google Scholar
  82. Shivvers, D. G., and Brock, T. D. (1973). J. Bacteriol. 114, 706-710.Google Scholar
  83. Sperling, D., Kappler, U., Trüper, H. G., and Dahl, C. (2001). Methods Enzymol. 331, 419-427.Google Scholar
  84. Stetter, K. O. (1982). Nature 300, 258-260.Google Scholar
  85. Stetter, K. O. (1988). Syst. Appl. Microbiol. 10, 172-173.Google Scholar
  86. Stetter, K. O. (1992). In Frontiers of Life. IIIrd Rencontres de Blois (Thanh Van, T., eds), Gif-sur-Yvette Cedex, France.Google Scholar
  87. Stetter, K. O., and Gaag, G. (1983). Nature 305, 309-311.Google Scholar
  88. Stetter, K. O., König, H., and Stackebrandt, E. (1983). Syst. Appl. Microbiol. 7, 393-397.Google Scholar
  89. Stetter, K. O., and Zillig, W. (1985). In The Bacteria, Vol VIII: A Treatise on Structure and Function: Archaebacteria (Woese, C. R., and Wolfe, R. S., eds.), Academic Press, Orlando, London, pp. 85-170.Google Scholar
  90. Steudel, R. (1996). Ind. Eng. Chem. Res. 35, 1417-1423.Google Scholar
  91. Stoiber, R. E. (1995). In Global Earth Physics: A Handbook of Physical Constants (Ahrens, T. J., ed.), American Geophysical Union, pp. 308-319.Google Scholar
  92. Strauss, G., Eisenreich, W., Bacher, A., and Fuchs, G. (1992). European Journal of Biochemistry 205, 853-866.Google Scholar
  93. Sun, C. W., Chen, Z. W., He, Z. G., Zhou, P. J., and Liu, S. J. (2003). Extremophiles 7, 131-134.Google Scholar
  94. Suzuki, I. (1965). Biochim. Biophys. Acta 110, 97-101.Google Scholar
  95. Suzuki, I., and Silver, M. (1966). Biochim. Biophys. Acta 127, 22-33.Google Scholar
  96. Symonds, B. R., Rose, W. I., Bluth, G. J. S., and Gerlach, T. M. (1994). In Volatiles in Magmas (Carroll, M. R., and Holloway, J. R., eds.), Mineralogical Society of America, pp. 1-66.Google Scholar
  97. Tano, T., and Imai, K. (1968). Agric. Biol. Chem. 32, 51-54.Google Scholar
  98. Teixeira, M., Batista, R., Campos, A., Gomes, C., Mendes, J., Pacheco, I., Anemuller, S., and Hagen, W. (1995). Eur. J. Biochem. 227, 322-327.Google Scholar
  99. Thauer, R. K., Jungermann, K., and Decker, K. (1977). Bacteriol. Rev. 41, 100-180.Google Scholar
  100. Theissen, U., Hoffmeister, M., Grieshaber, M., and Martin, W. (2003). Mol. Biol. Evol. MBE Advance Access published June 27, 2003, 10.1093/molbev/msg174Google Scholar
  101. Trincone, A., Lanzotti, V., Nicolaus, B., Zillig, W., Derosa, M., and Gambacorta, A. (1989). J. Gen. Microbiol. 135, 2751-2757.Google Scholar
  102. Visser, J. M., de Jong, G. A. H., Robertson, L. A., and Kuenen, J. G. (1997). Arch. Microbiol. 166, 372-378.Google Scholar
  103. Völkl, P., Huber, R., Brobner, E., Rachel, R., Burggraf, S., Trincone, A., and Stetter, K. O. (1993). Appl. Environ. Microbiol. 59, 2918-2926.Google Scholar
  104. Xu, Y., Schoonen, M. A. A., Nordstrom, D. K., Cunningham, K. M., and Ball, J. W. (1998). Geochim. Cosmochim. Acta 62, 3729-3743.Google Scholar
  105. Xu, Y., Schoonen, M. A. A., Nordstrom, D. K., Cunningham, K. M., and Ball, J. W. (2000). J. Volcanol. Geotherm. Res. 97, 407-423.Google Scholar
  106. Zellner, G., Stackebrandt, E., Kneifel, H., Messner, P., Sleytr, U. B., Conway, E., Zabel, H.-P., Stetter, K. O., and Winter, J. (1989). Syst. Appl. Microbiol. 11, 151-160.Google Scholar
  107. Zillig, W., Stetter, K. O., Wunderl, S., Schulz, W., Priess, H., and Scholz, I. (1980). Arch. Microbiol. 125, 259-269.Google Scholar
  108. Zillig, W., Tu, J., and Holz, I. (1981). Nature 293, 85-86.Google Scholar
  109. Zillig, W., Yeats, S., Holz, I., Böck, A., Gropp, F., Rettenberger, M., and Lutz, S. (1985). Nature 313, 789-791.Google Scholar
  110. Zillig, W., Yeats, S., Holz, I., Böck, A., Rettenberger, M., Gropp, F., and Simon, G. (1986). Syst. Appl. Microbiol. 8, 197-203.Google Scholar
  111. Zimmermann, P., Laska, S., and Kletzin, A. (1999). Arch. Microbiol. 172, 76-82.Google Scholar

Copyright information

© Plenum Publishing Corporation 2004

Authors and Affiliations

  • Arnulf Kletzin
    • 1
  • Tim Urich
    • 1
  • Fabian Müller
    • 1
  • Tiago M. Bandeiras
    • 2
  • Cláudio M. Gomes
    • 2
    • 3
  1. 1.Institute of Microbiology and GeneticsDarmstadt University of TechnologyDarmstadtGermany
  2. 2.Instituto de Tecnologia Química e Biológica, Universidade Nova de LisboaOeirasPortugal
  3. 3.Departamento de Química, Faculdade de Ciências e TecnologiaUniversidade Nova de LisboaCaparicaPortugal

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