A succinate dehydrogenase with novel structure and properties from the hyperthermophilic archaeon Sulfolobus acidocaldarius: Genetic and biophysical characterization

Journal of Bacteriology

Volumn 179, Issue 17, 1997, Pages 5560-5569

  Janssen, Silke ^a   Schäfer, Günter ^a   Anemüller, Stefan ^a   Moll, Ralf ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SUCCINATE DEHYDROGENASE;

ALPHA HELIX; ARTICLE; BACTERIAL MEMBRANE; CITRIC ACID CYCLE; COVALENT BOND; ELECTRON SPIN RESONANCE; ENZYME PURIFICATION; GRAM NEGATIVE BACTERIUM; NONHUMAN; OPERON; PRIORITY JOURNAL; RESPIRATORY CHAIN; SITE DIRECTED MUTAGENESIS; START CODON; SURFACE PROPERTY;

ARCHAEA; BACTERIA (MICROORGANISMS); METHANOBACTERIUM; METHANOCALDOCOCCUS JANNASCHII; METHANOCOCCUS; METHANOTHERMOBACTER THERMAUTOTROPHICUS; NEGIBACTERIA; SULFOLOBUS ACIDOCALDARIUS;

EID: 1842332148     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.17.5560-5569.1997     Document Type: Article

References (65)

1. Aasa, R., and T. Vänngärd. 1975. EPR signal intensity and powder shapes: a reexamination. J. Magn. Reson. 19:308-315.
2. Ackrell, B. A. C., M. K. Johnson, R. P. Gunsalus, and G. Cecchini. 1992. Structure and function of succinate dehydrogenase and fumarate reductase, p. 229-297. In F. Müller (ed.), Chemistry and biochemistry of flavoenzymes, vol. 3. CRC Press, London, England.
3. Aevarsson, A., and L. Hederstedt. 1988. Ligands of the 2 Fe iron-sulfur center in succinate dehydrogenases. FEBS Lett. 232:298-302.
4. Anemüller, S., T. Hettmann, R. Moll, M. Teixeira, and G. Schäfer. 1995. EPR characterization of an archaeal succinate dehydrogenase in the membrane-bound state. Eur. J. Biochem. 232:563-568.
5. Bach, M., H. Reiländer, P. Gärtner, F. Lottspeich, and H. Michel. 1993. Nucleotide sequence of a putative succinate dehydrogenase operon in Thermoplasma acidophilum. Biochim. Biophys. Acta 1174:103-107.
6. Birnboim, H. C., and J. Doly. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 7:1513.
7. 3-phosphate. J. Biol. Chem. 264:18714-18718.
8. Boehringer Mannheim GmbH. 1993. The DIG system user's guide for filter hybridization. Boehringer Mannheim GmbH, Mannheim, Germany.
9. Brown, J. D., C. Daniels, and J. N. Reeve. 1989. Gene structure, organization and expression in archaebacteria. Crit. Rev. Microbiol. 16:287-338.
10. Cecchini, G., H. Sices, I. Schröder, and R. P. Gunsalus. 1995. Aerobic inactivation of fumarate reductase from Escherichia coli by mutation of the [3Fe4S]-quinone binding domain. J. Bacteriol. 177:4587-4592.
11. Chomczynski, P. 1992. One-hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal. Biochem. 201:134-139.
12. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
13. Cole, S. T., C. Codon, B. D. Lemire, and J. H. Weiner. 1985. Molecular biology, biochemistry and bioenergetics of fumarate reductase, a complex membrane-bound iron-sulfur flavoenzyme of Escherichia coli. Biochim. Biophys. Acta 811:381-403.
14. Dunn, R., J. McCoy, M. Simsek, A. Majumdar, S. H. Chang, U. L. Rajbhandary, and H. G. Khorana. 1981. The bacteriorhodopsin gene. Proc. Natl. Acad. Sci. USA 78:6744-6748.
15. Engelmann, D. M., T. A. Steitz, and A. Goldman. 1986. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu. Rev. Biophys. Chem. 15:321-353.
16. Gradin, C. H., L. Hederstedt, and H. Baltscheffsky. 1985. Soluble succinate dehydrogenase from the halophilic archaebacterium Halobacterium halobium. Arch. Biochem. Biophys, 239:200-205.
17. Hägerhäll, C. 1997. Succinate:quirone oxidoreductases; variations on a conserved theme. Biochim. Biophys. Acta 1320:107-141.
18. Hägerhäll, C., R. Aasa, C. v. Wachenfeldt, and L. Hederstedt. 1992. Two hemes in Bacillus subtilis succinate:menaquinone oxidoreductase (complex II). Biochemistry 31:7411-7421.
19. Hägerhäll, C., and L. Hederstedt. 1996. A structural model for the membrane-integral domain of succinate:quinone oxidoreductases. FEBS Lett. 389:25-31.
20. Hägerhäll, C., V. Sled, L. Hederstedt, and T. Ohnishi. 1995. The trinuclear iron-sulfur cluster S3 in Bacillus subtilis succinate:menaquinone reductase; effects of a mutation in the putative cluster ligation motif on enzyme activity and EPR properties. Biochim. Biophys. Acta 1229:356-362.
21. Hedderich, R., and S. Heim. 1997. Personal communication.
22. Hedderich, R., J. Koch, and R. K. Thauer. 1994. The heterodisulfide reductase from Methanobacterium thermoautotrophicum contains sequence motifs characteristic of pyridine-nucleotide-dependent thioredoxin reductases. Eur. J. Biochem. 225:253-261.
23. Hederstedt, L., and L. Heden. 1989. New properties of Bacillus subtilis succinate dehydrogenase altered at the active site. Biochem. J. 260:491-497.
24. Hederstedt, L., and T. Ohnishi. 1992. Progress in succinate:quinone oxidoreductase research, p. 163-198. In L. Ernster (ed.), Molecular mechanisms in bioenergetics. Elsevier Science, Amsterdam, The Netherlands.
25. Inoue, H., H. Nojiama, and H. Okajama. 1990. High efficiency transformation of Escherichia coli with plasmids. Gene 6:23-28.
26. Iwasaki, T., T. Wakagi, and T. Oshima. 1995. Resolution of the aerobic respiratory system of the thermoacidophilic archaeon, Sulfolobus sp. strain 7. J. Biol. Chem. 270:30902-30908.
27. Johnson, M. K., A. T. Kowal, T. E. Morningstar, M. E. Oliver, K. Whittaker, P. Gunsalus, B. A. C. Ackrell, and G. Cecchini. 1988. Subunit location of the iron sulfur clusters in fumarate reductase from Escherichia coli. J. Biol. Chem. 263:14732-14738.
28. Keeling, P. J., and W. F. Doolittle. 1995. Archaea: narrowing the gap between prokaryotes and eukaryotes. Proc. Natl. Acad. Sci. USA 92:5761-5764.
29. Kenny, W. C., and A. Kröger. 1977. The covalently bound flavin of Vibrio succinogenes succinate dehydrogenase. FEBS Lett. 73:239-243.
30. Kletzin, A. 1992. Molecular characterization of a DNA ligase gene of the extremely thermophilic archaeon Desulfurolobus ambivalens shows close phylogenetic relationship to eukaryotic ligases. Nucleic Acids Res. 20:5389-5398.
31. Kletzin, A. 1992. Molecular characterization of the sor gene, which encodes the sulfur oxygenase/reductase of the thermophilic archaeum Desulfurolobus ambivalens. J. Bacteriol. 174:5854-5859.
32. Körtner, C., F. Lauterbach, D. Tripier, G. Unden, and A. Kröger. 1990. Wolinella succinogenes fumarate reductase contains a dihaem cytochrome b. Mol. Microbiol. 4:855-860.
33. Künkel, A., M. Vaupel, S. Heim, R. K. Thauer, and R. Hedderich. 1997. Heterodisulfide reductase from methanol grown cells of Methanosarcina barkeri is not a flavoenzyme. Eur. J. Biochem. 244:226-234.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Lauterbach, F., C. Körtner, S. P. J. Albracht, G. Unden, and A. Kröger. 1990. The fumarate reductase operon of Wolinella succinogenes. Arch. Microbiol. 154:386-393.
36. Maguire, J. J., and L. Hederstedt. 1989. EPR characterization of the soluble fragments of succinate dehydrogenase from mutant strains of Bacillus subtilis. FEMS Lett. 256:195-199.
37. Manodori, A., G. Cecchini, I. Schröder, R. P. Gunsalus, M. Werth, and M. K. Johnson. 1992. [3Fe4S] to [4Fe4S] cluster conversion in Escherichia coli fumarate reductase by site-directed mutagenesis. Biochemistry 31:2703-2712.
38. Marmur, J. 1961. A procedure for the isolation of desoxyribonucleic acid from microorganisms. J. Mol. Biol. 3:208-218.
39. Moll, R., and G. Schäfer. 1989. Membrane-bound succinate dehydrogenase activity in the thermoacidophilic archaebacterium Sulfolobus acidocaldarius. Biol. Chem. Hoppe-Seyler 370:936-937.
40. Moll, R., and G. Schäfer. 1991. Purification and characterization of an archaebacterial succinate dehydrogenase complex from the plasma membrane of the thermoacidophile Sulfolobus acidocaldarius. Eur. J. Biochem. 201:593-600.
41. Morningstar, J. E., M. K. Johnson, G. Cecchini, B. A. C. Ackrell, and E. B. Kearny. 1985. The high potential iron-sulfur center in Escherichia coli fumarate reductase is a three-iron cluster. J. Biol. Chem. 260:13631-13638.
42. Morris, A. A. M., L. Farnsworth, B. A. C. Ackrell, S. Turnbull, M., and M. A. Birch-Machin. 1994. The cDNA sequence of the flavoprotein subunit of human heart succinate dehydrogenase. Biochim. Biophys. Acta 1185:125-128.
43. Nakamura, K., M. Yamaki, M. Sarada, S. Nakayama, C. R. T. Vibat, R. B. Gennis, T. Nakayashiki, H. Inokuchi, S. Kojima, and K. Kita. 1996. Two hydrophobic subunits are essential for the heme b ligation and functional assembly of complex II (succinate-ubiquinone oxidoreductase) from Escherichia coli. J. Biol. Chem. 271:521-527.
44. Peterson, J., C. Vibat, and R. B. Gennis. 1994. Identification of the axial heme ligands of cytochrome b556 in succinate:ubiquinone oxidoreductase from Escherichia coli. FEBS Lett. 355:155-156.
45. Purschke, W. G., and G. Schäfer. 1996. An alternative to digoxigenin-labeled primers for manual nonradioactive sequencing allows reading of more than 700 bases. Anal. Biochem. 238:98-100.
46. Reiter, W. D., P. Palm, and W. Zillig. 1988. Transcription termination in the archacbacterium Sulfolobus: signal structures and linkage to transcription initiation. Nucleic Acids Res. 16:2445-2459.
47. Rice, D. W., G. E. Schultz, and J. R. Guest. 1984. Structural relationship between glutathione reductase and lipoamide dehydrogenase. J. Mol. Biol. 174:483-496.
48. Sambrook, S., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
49. Schäfer, G. 1996. Bioenergetics of the archaebacterium Sulfolobus. Biochim. Biophys. Acta 1277:163-200.
50. Schäfer, G., W. G. Purschke, M. Gleissner, and C. L. Schmidt. 1996. Respiratory chains of archaea and extremophiles. Biochim. Biophys. Acta 1275: 16-20.
51. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
52. Schmitz, G. G., T. Walter, R. Seibl, and C. Kessler. 1991. Nonradioactive labeling of oligonucleotides in vitro with hapten digoxigenin by tailing with terminal transferase. Anal. Biochem. 192:222-231.
53. Schröder, I., and R. P. Gunsalus. 1991. Identification of active site residues of Escherichia coli fumarate reductase by site-directed mutagenesis. J. Biol. Chem. 266:13572-13579.
54. Setzke, E., R. Hedderich, S. Heiden, and R. K. Thauer. 1994. H2:heterodisulfide oxidoreductase complex from Methanobacterium thermoautotrophicum. Composition and properties. Eur. J. Biochem. 220:139-148.
55. Smirnova, I., C. Hägerhäll, A. A. Konstantinov, and L. Hederstedt. 1995. HOQNO interaction with cytochrome b in succinate:menaquinone oxidoreductase from Bacillus subtilis. FEBS Lett. 359:23-26.
56. Thomas, M., and G. Wich. 1988. An archaeal promoter element for stable RNA genes with homology to the TATA box of higher eukaryotes. Nucleic Acids Res. 16:151-163.
57. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
58. Vik, S. B., and Y. Hatefi. 1981. Possible occurrence and role of an essential histidyl residue in succinate dehydrogenase. Proc. Natl. Acad. Sci. USA 78:6749-6753.
59. Vinogradov, A. D., E. V. Gavrikova, and V. V. Zuevsky. 1976. Reactivity of the sulfhydryl groups of soluble succinate dehydrogenase. Eur. J. Biochem. 63:365-371.
60. Walker, W. H., and T. P. Singer. 1970. Identification of the covalently-bound flavin of succinate dehydrogenase as 8α-(histidyl) flavin adenin dinucleotide. J. Biol. Chem. 245:4224-4225.
61. Weiner, J. H., and P. Dickie. 1979. Fumarate reductase of Escherichia coli. Elucidation of the covalent-flavin component. J. Biol. Chem. 254:8590-8593.
62. Werth, M. T., G. Cecchini, A. Mandori, B. A. C. Ackrell, I. Schröder, R. P. Gunsalus, and K. Johnson. 1990. Site-directed mutagenesis of conserved cysteine residues in Escherichia coli fumarate reductase: modification of the spectroscopic and electrochemical properties of the [2Fe2S] cluster. Proc. Natl. Acad. Sci. USA 87:8965-8969.
63. Westenberg, D. J., R. P. Gunsalus, B. A. C. Ackrell, and G. Cecchini. 1990. Electron transfer from menaquinone to fumarate. Fumarate reductase anchor polypeptide mutants of Escherichia coli. J. Biol. Chem. 265:19560-19567.
64. Westenberg, D. J., R. P. Gunsalus, B. A. C. Ackrell, H. Sices, and G. Cecchini. 1993. Escherichia coli fumarate reductase frdC and frdD mutants. Identification of amino acid residues involved in catalytic activity with quinones. J. Biol. Chem. 268:815-822.
65. Wierenga, R. K., P. Terpstra, and G. J. Hol. 1986. Prediction of the occurrence of the ADP-binding βαβ-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187:101-107.