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Dissimilatory Oxidation and Reduction of Elemental Sulfur in Thermophilic Archaea

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Abstract

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.

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References

  • Aagaard, A., Gilderson, G., Gomes, C. M., Teixeira, M., and Brzezinski, P. (1999). Biochemistry. 38, 10032-10041.

    Google Scholar 

  • 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 

  • Amend, J. P., and Shock, E. L. (2001). FEMS Microbiol. Rev. 25, 175-243.

    Google Scholar 

  • Arendsen, A. F., Veenhuizen, P. T., and Hagen, W. R. (1995). FEBS Lett. 368, 117-121.

    Google Scholar 

  • Bandeiras, T. M., Salgueiro, C., Kletzin, A., Gomes, C. M., Teixeira, M. (2002). FEBS Lett. 531, 273-277.

    Google Scholar 

  • Barns, S. M., Fundya, R. E., Jeffries, M. W., and Pace, N. R. (1994). Proc. Natl. Acad. Sci. 91, 1609-1613.

    Google Scholar 

  • Blamey, J. M., and Adams, M. W. W. (1993). Biochim. Biophys. Acta 1161, 19-27.

    Google Scholar 

  • 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 

  • Brierley, C. L., and Brierley, J. A. (1973). Can. J. Microbiol. 19, 183-188.

    Google Scholar 

  • Brierley, C. L., and Brierley, J. A. (1982). Zbl. Bakt. Hyg., I. Abt. Orig. C 3, 289-294.

    Google Scholar 

  • Brock, T. D., Brock, K. M., Belly, R. T., and Weiss, R. L. (1972). Arch. Microbiol. 84, 54-68.

    Google Scholar 

  • Brüser, T., Selmer, T., and Dahl, C. (2000). J. Biol. Chem. 275, 1691-1698.

    Google Scholar 

  • Bryant, F. O., and Adams, M. W. (1989). J. Biol. Chem. 264, 5070-5079.

    Google Scholar 

  • Dahl, C., Molitor, M., and Trüper, H. G. (2001). Methods Enzymol. 331, 410-419.

    Google Scholar 

  • Dahl, C., and Trüper, H. G. (2001). Methods Enzymol. 331, 427-441.

    Google Scholar 

  • Daniels, L., Belay, N., and Rajagopal, B. S. (1986). Appl. Environ. Microbiol. 51, 703-709.

    Google Scholar 

  • Das, T. K., Gomes, C. M., Teixeira, M., and Rousseau, D. L. (1999). Proc. Natl. Acad. Sci. U.S.A. 96, 9591-9596

    Google Scholar 

  • Dietrich, W., and Klimmek, O. (2002). Eur. J. Biochem. 269, 1086-1095.

    Google Scholar 

  • Dirmeier, R., Keller, M., Frey, G., Huber, H., and Stetter, K. O. (1998). Eur. J. Biochem. 252, 486-491.

    Google Scholar 

  • Emmel, T., Sand, W., König, W. A., and Bock, E. (1986). J. Gen. Microbiol. 132, 3415-3420.

    Google Scholar 

  • Fischer, F., Zillig, W., Stetter, K. O., and Schreiber, G. (1983). Nature 301, 511-513.

    Google Scholar 

  • Friedrich, C. G. (1998). Adv. Microb. Physiol. 39, 235-289.

    Google Scholar 

  • Friedrich, C. G., Rother, D., Bardischewsky, F., Quentmeier, A., and Fischer, J. (2001). Appl. Environ. Microbiol. 67, 2873-2882.

    Google Scholar 

  • 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 

  • Fuchs, T., Huber, H., Burggraf, S., and Stetter, K. O. (1996). Syst. Appl. Microbiol. 19, 56-60.

    Google Scholar 

  • Gomes, C. M. (1999). In Instituto Tecnologia Química e Biológica, PhD Thesis, Universidade Nova de Lisboa, Oeiras.

    Google Scholar 

  • 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 

  • Gomes, C. M., Bandeiras, T. M., and Teixeira, M. (2001b). J. Bioenerg. Biomembr. 33, 1-8.

    Google Scholar 

  • 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 

  • Griesbeck, C., Schutz, M., Schodl, T., Bathe, S., Nausch, L., Mederer, N., Vielreicher, M., and Hauska, G. (2002). Biochemistry 41, 11552-11565.

    Google Scholar 

  • Grogan, D. W. (1989). J. Bacteriol. 171, 6710-6719.

    Google Scholar 

  • He, Z., Li, Y., Zhou, P., and Liu, S. (2000). FEMS Microbiol. Lett. 193, 217-221.

    Google Scholar 

  • Hedderich, R., Klimmek, O., Kröger, A., Dirmeier, R., Keller, M., and Stetter, K. O. (1999). FEMS Microbiol. Rev. 22, 353-381.

    Google Scholar 

  • Hellwig, P., Gomes, C. M., and Teixeira, M. (2003). Biochemistry 42, 6179-6184.

    Google Scholar 

  • 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 

  • Holland, H. D. (2002). Geochim. Cosmochim. Acta 66, 3811-3826.

    Google Scholar 

  • Huber, G., Drobner, E., Huber, H., and Stetter, K. O. (1992). Syst. Appl. Microbiol. 15, 502-504.

    Google Scholar 

  • Huber, R., Kristiansson, J. K., and Stetter, K. O. (1987). Arch. Microbiol. 149, 95-101.

    Google Scholar 

  • Hugler, M., Huber, H., Stetter, K. O., and Fuchs, G. (2003). Arch. Microbiol. 179, 160-173.

    Google Scholar 

  • Ishii, M., Miyake, T., Satoh, T., Sugiyama, H., Oshima, Y., Kodama, T., and Igarashi, Y. (1996). Arch. Microbiol. 166, 368-371.

    Google Scholar 

  • Kanai, T., Ito, S., and Imanaka, T. (2003). J. Bacteriol. 185, 1705-1711.

    Google Scholar 

  • Kappler, U., and Dahl, C. (2001). FEMS Microbiol. Lett. 203, 1-9.

    Google Scholar 

  • Kelly, D. P. (1982). Philos. Trans. R. Soc., Lond. Ser. B 298, 499-528.

    Google Scholar 

  • 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 

  • Kelly, D. P., Shergill, J. K., Lu, W. P., and Wood, A. P. (1997). Antonie Van Leeuwenhoek 71, 95-107.

    Google Scholar 

  • Kelly, D. P., and Wood, A. P. (1994). Methods Enzymol. 243, 501-510.

    Google Scholar 

  • Kengen, S. W. M., and Stams, A. J. M. (1994). FEMS Microbiol. Lett. 117, 305-309.

    Google Scholar 

  • 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 

  • Kletzin, A. (1989). J. Bacteriol. 171, 1638-1643.

    Google Scholar 

  • Kletzin, A. (1992). J. Bacteriol. 174, 5854-5859.

    Google Scholar 

  • Kletzin, A. (1994). Syst. Appl. Microbiol. 16, 534-543.

    Google Scholar 

  • Larsson, L., Olsson, G., Holst, O., and Karlsson, H. T. (1990). Appl. Environ. Microbiol. 56, 697-701.

    Google Scholar 

  • Laska, S., and Kletzin, A. (2000). J. Chromatogr. B 737, 151-160.

    Google Scholar 

  • Laska, S., Lottspeich, F., and Kletzin, A. (2003). Microbiology 149, 2357-2371.

    Google Scholar 

  • Le Faou, A., Rajagopal, B. S., Daniels, L., and Fauque, G. (1990). FEMS Microbiol. Rev. 6, 351-381.

    Google Scholar 

  • Lemos, R. S., Gomes, C. M., and Teixeira, M. (2001). Biochem. Biophys. Res. Comm., 281, 141-150.

    Google Scholar 

  • Ma, K., and Adams, M. W. (1994). J. Bacteriol. 176, 6509-6517.

    Google Scholar 

  • Ma, K., and Adams, M. W. (2001). Methods Enzymol. 331, 208-216.

    Google Scholar 

  • 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 

  • Ma, K., Weiss, R., and Adams, M. W. (2000). J. Bacteriol. 182, 1864-1871.

    Google Scholar 

  • Montegrossi, G., Tassi, F., Vaselli, O., Buccianti, A., and Garofalo, K. (2001). Anal. Chem., 73, 3709-3715.

    Google Scholar 

  • Mukund, S., and Adams, M. W. W. (1995). J. Biol. Chem. 270, 8389-8392.

    Google Scholar 

  • Nakamura, K., Nakamura, M., Yoshikawa, H., and Amano, Y. (2001). Biosci. Biotechnol. Biochem. 65, 102-108.

    Google Scholar 

  • Pihl, T. D., Black, L. K., Schulman, B. A., and Maier, R. J. (1992). J. Bacteriol. 174, 137-143.

    Google Scholar 

  • Pihl, T. D., and Maier, R. J. (1991). J. Bacteriol. 173, 1839-1844.

    Google Scholar 

  • 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 

  • 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 

  • Pronk, J. T., Meulenberg, R., Hazeu, W., Bos, P., and Kuenen, J. G. (1990). FEMS Microbiol. Rev. 75, 293-306.

    Google Scholar 

  • Purschke, W. G., Schmidt, C. L., Petersen, A., and Schäfer, G. (1997). J. Bacteriol. 179, 1344-1353.

    Google Scholar 

  • Quentmeier, A., and Friedrich, C. G. (2001). FEBS Lett. 503, 168-172.

    Google Scholar 

  • Reysenbach, A. L., Wickham, G. S., and Pace, N. R. (1994). Appl. Environ. Microbiol. 60, 2113-2119.

    Google Scholar 

  • Rother, D., Henrich, H. J., Quentmeier, A., Bardischewsky, F., and Friedrich, C. G. (2001). J. Bacteriol. 183, 4499-4508.

    Google Scholar 

  • Sapra, R., Bagramyan, K., and Adams, M. W. (2003). Proc. Natl. Acad. Sci. U.S.A. 100, 7545-7550.

    Google Scholar 

  • Sapra, R., Verhagen, M. F., and Adams, M. W. (2000). J. Bacteriol. 182, 3423-3428.

    Google Scholar 

  • Schäfer, A., Barkowski, C., and Fuchs, G. (1986). Arch. Microbiol. 146, 301-308.

    Google Scholar 

  • Schauder, R., and Kröger, A. (1993). Arch. Microbiol. 159, 491-497.

    Google Scholar 

  • Schicho, R. N., Ma, K., Adams, M. W., and Kelly, R. M. (1993). J. Bacteriol. 175, 1823-1830.

    Google Scholar 

  • Schönheit, P., and Schäfer, T. (1995). World J. Microbiol. Biotechnol. 11, 26-57.

    Google Scholar 

  • Schut, G., Zhou, J., and Adams, M. (2001). J. Bacteriol. 183, 7027-7036.

    Google Scholar 

  • Segerer, A., Stetter, K. O., and Klink, F. (1985). Nature 313, 787-789.

    Google Scholar 

  • Selig, M., and Schönheit, P. (1994). Arch. Microbiol. 162, 286-294.

    Google Scholar 

  • Shivvers, D. G., and Brock, T. D. (1973). J. Bacteriol. 114, 706-710.

    Google Scholar 

  • Sperling, D., Kappler, U., Trüper, H. G., and Dahl, C. (2001). Methods Enzymol. 331, 419-427.

    Google Scholar 

  • Stetter, K. O. (1982). Nature 300, 258-260.

    Google Scholar 

  • Stetter, K. O. (1988). Syst. Appl. Microbiol. 10, 172-173.

    Google Scholar 

  • Stetter, K. O. (1992). In Frontiers of Life. IIIrd Rencontres de Blois (Thanh Van, T., eds), Gif-sur-Yvette Cedex, France.

    Google Scholar 

  • Stetter, K. O., and Gaag, G. (1983). Nature 305, 309-311.

    Google Scholar 

  • Stetter, K. O., König, H., and Stackebrandt, E. (1983). Syst. Appl. Microbiol. 7, 393-397.

    Google Scholar 

  • 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 

  • Steudel, R. (1996). Ind. Eng. Chem. Res. 35, 1417-1423.

    Google Scholar 

  • Stoiber, R. E. (1995). In Global Earth Physics: A Handbook of Physical Constants (Ahrens, T. J., ed.), American Geophysical Union, pp. 308-319.

  • Strauss, G., Eisenreich, W., Bacher, A., and Fuchs, G. (1992). European Journal of Biochemistry 205, 853-866.

    Google Scholar 

  • Sun, C. W., Chen, Z. W., He, Z. G., Zhou, P. J., and Liu, S. J. (2003). Extremophiles 7, 131-134.

    Google Scholar 

  • Suzuki, I. (1965). Biochim. Biophys. Acta 110, 97-101.

    Google Scholar 

  • Suzuki, I., and Silver, M. (1966). Biochim. Biophys. Acta 127, 22-33.

    Google Scholar 

  • 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.

  • Tano, T., and Imai, K. (1968). Agric. Biol. Chem. 32, 51-54.

    Google Scholar 

  • 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 

  • Thauer, R. K., Jungermann, K., and Decker, K. (1977). Bacteriol. Rev. 41, 100-180.

    Google Scholar 

  • Theissen, U., Hoffmeister, M., Grieshaber, M., and Martin, W. (2003). Mol. Biol. Evol. MBE Advance Access published June 27, 2003, 10.1093/molbev/msg174

  • Trincone, A., Lanzotti, V., Nicolaus, B., Zillig, W., Derosa, M., and Gambacorta, A. (1989). J. Gen. Microbiol. 135, 2751-2757.

    Google Scholar 

  • Visser, J. M., de Jong, G. A. H., Robertson, L. A., and Kuenen, J. G. (1997). Arch. Microbiol. 166, 372-378.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • Zillig, W., Stetter, K. O., Wunderl, S., Schulz, W., Priess, H., and Scholz, I. (1980). Arch. Microbiol. 125, 259-269.

    Google Scholar 

  • Zillig, W., Tu, J., and Holz, I. (1981). Nature 293, 85-86.

    Google Scholar 

  • Zillig, W., Yeats, S., Holz, I., Böck, A., Gropp, F., Rettenberger, M., and Lutz, S. (1985). Nature 313, 789-791.

    Google Scholar 

  • Zillig, W., Yeats, S., Holz, I., Böck, A., Rettenberger, M., Gropp, F., and Simon, G. (1986). Syst. Appl. Microbiol. 8, 197-203.

    Google Scholar 

  • Zimmermann, P., Laska, S., and Kletzin, A. (1999). Arch. Microbiol. 172, 76-82.

    Google Scholar 

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Kletzin, A., Urich, T., Müller, F. et al. Dissimilatory Oxidation and Reduction of Elemental Sulfur in Thermophilic Archaea. J Bioenerg Biomembr 36, 77–91 (2004). https://doi.org/10.1023/B:JOBB.0000019600.36757.8c

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