Cloning and characterization of sulfite dehydrogenase, two c-type cytochromes, and a flavoprotein of Paracoccus denitrificans GB17: Essential role of sulfite dehydrogenase in lithotrophic sulfur oxidation

Journal of Bacteriology

Volumn 179, Issue 16, 1997, Pages 5014-5023

  Wodara, Christoph ^a,b   Bardischewsky, Frank ^b   Friedrich, Cornelius G ^b  

^a Universität Dortmund ^*  (Germany)

^b TU DORTMUND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME; FLAVOPROTEIN; OXIDOREDUCTASE; SULFITE;

ARTICLE; BACTERIAL METABOLISM; ENZYME ACTIVITY; MOLECULAR CLONING; NONHUMAN; PARACOCCUS DENITRIFICANS; PRIORITY JOURNAL;

ALLOCHROMATIUM VINOSUM; BACTERIA (MICROORGANISMS); CHROMATIUM; EUKARYOTA; PARACOCCUS DENITRIFICANS;

EID: 0030843666     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.16.5014-5023.1997     Document Type: Article

References (59)

1. Ambler, R. P., T. E. Meyer, P. A. Trudinger, and M. D. Kamen. 1985. The amino acid sequence of the cytochrome c-554(547) from the chemolithotrophic bacterium Thiobacillus neapolitanus. Biochem. J. 227:1009-1013.
2. 2: close similarity to functionally unrelated mitochondrial cytochrome c. Proc. Natl. Acad. Aci. USA 73:472-475.
3. Barber, M. J., and P. J. Neame. 1990. A conserved cysteine in molybdenum oxotransferases. J. Biol. Chem. 265:20912-20915.
4. Beijerinck, M., and D. C. J. Minkman. 1910. Bildung und Verbrauch von Stickoxydul durch Bakterien. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Abt. 2 25:30-63.
5. Bokranz, M., M. Gutmann, C. Körtner, E. Kojro, F. Fahrenholz, F. Lauterbach, and A. Kröger. 1991. Cloning and nucleotide sequence of the structural genes encoding the formate dehydrogenase of Wolinella succinogenes. Arch. Microbiol. 156:119-128.
6. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
7. Bullock, W. O., J. M. Fernandez, and J. M. Short. 1987. XL1-Blue: a high efficiency plasmid transforming recA Escherichia coli strains with beta-galactosidase selection. BioTechniques 5:376-378.
8. Chandra, T. S., and C. G. Friedrich. 1986. Tn5-induced mutations affecting sulfur-oxidizing ability (Sox) of Thiosphaera pantotropha. J. Bacteriol. 166: 446-452.
9. Chen, Z.-W., M. Koh, G. van Driessche, J. J. Van Beeumen, R. G. Bartsch, T. E. Meyer, M. A. Cusanovich, and F. C. Mathews. 1994. The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium. Science 266:430-432.
10. Crawford, N. M., M. Smith, D. Bellissimo, and R. W. Davis. 1988. Sequence and nitrate regulation of the Arabidopsis thaliana mRNA encoding nitrate reductase, a metalloflavoprotein with three functional domains. Proc. Natl. Acad. Sci. USA 85:5006-5010.
11. Daniel-Vedele, F., M. F. Dorbe, M. Caboche, and P. Rouzé. 1989. Cloning and analysis of the tomato nitrate-reductase-encoding gene: protein domain structure and amino acid homologies in higher plants. Gene 85:371-380.
12. Dernedde, J., T. Eitinger, N. Patenge, and B. Friedrich. 1996. hyp gene products in Alcaligenes eutrophus are part of a hydrogenase-maturation system. Eur. J. Biochem. 235:351-358.
13. Dolata, M. M., J. J. Van Beeumen, R. P. Ambler, T. E. Meyer, and M. A. Cusanovich. 1993. Nucleotide sequence of the heme subunit of flavocytochrome c from the purple phototrophic bacterium Chromatium vinosum. A 2.6-kilobase pair fragment contains two multiheme cytochromes, a flavoprotein, and a homolog of human ankyrin. J. Biol. Chem. 268:14426-14431.
14. Fischer, J., A. Quentmeier, S. Kostka, R. Kraft, and C. G. Friedrich. 1996. Purification and characterization of the hydrogenase from Thiobacillus ferrooxidans. Arch. Microbiol. 165:289-296.
15. Friedrich, B., and E. Schwartz. 1993. Molecular biology of hydrogen utilization in aerobic chemolithotrophs. Annu. Rev. Microbiol. 47:351-383.
16. Friedrich, C. 1997. Physiology and genetics of sulfur-oxidizing bacteria. Adv. Microb. Physiol. 39:235-289.
17. Friedrich, C. G., and G. Mitrenga. 1981. Oxidation of thiosulfate by Paracoccus denitrificans and other hydrogen bacteria. FEMS Microbiol. Lett. 10:209-212.
18. Friedrich, C. G., O. Meyer, and T. S. Chandra. 1986. Molybdenum dependent sulfur oxidation in facultatively lithoautotrophic thiobacteria. FEMS Microbiol. Lett. 37:105-108.
19. Fukumori, Y. P., and I. Yamanaka. 1979. Flavocytochrome c of Chromatium vinosum. Some enzymatic properties and subunit structure. J. Biochem. (Tokyo) 85:1405-1414.
20. Garrett, R. M., D. B. Bellissimo, and K. V. Rajagopalan. 1995. Molecular cloning of human liver sulfite oxidase. Biochim. Biophys. Acta 1262:147-149.
21. Garrett, R. M., and K. V. Rajagopalan. 1994. Molecular cloning of rat liver sulfite oxidase. J. Biol. Chem. 269:272-276.
22. 2 gene. J. Bacteriol. 172:5071-5078.
23. Katayama, Y., A. Hiraishi, and H. Kuraishi. 1995. Paracoccus thiocyanatus sp. nov., a new species of thiocyanate-utilizing facultative chemolithotroph, and transfer of Thiobacillus versutus to the genus Paracoccus as Paracoccus versutus comb. nov. with emendation of the genus. Microbiology 141:1469-1477.
24. Kelly, D. P. 1989. Physiology and biochemistry of unicellular sulfur bacteria, p. 193-217. In H. G. Schlegel and B. Bowien (ed.), Autotrophic bacteria. Brock/Springer, Berlin, Germany.
25. Kluyver, A. J., and W. Verhoeven. 1954. Studies on true nitrate reduction. IV. On adaptation in Micrococcus denitrificans. Antonie Leeuwenhoek J. Microbiol. Serol. 20:337-358.
26. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
27. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
28. Lu, W.-P. 1986. A periplasmic location for the thiosulfate-oxidizing multienzyme system from Thiobacillus versutus. FEMS Microbiol. Lett. 34:313-317.
29. Lu, W.-P., and D. P. Kelly. 1984. Properties and role of sulfite:cytochrome c oxido-reductase purified from Thiobacillus versutus (A2). J. Gen. Microbiol. 130:1683-1692.
30. Ludwig, W., G. Mittenhuber, and C. G. Friedrich. 1993. Transfer of Thiosphaera pantotropha to Paracoccus denitrificans. Int. J. Syst. Bacteriol. 43: 363-367.
31. Maier, T., and A. Böck. 1996. Nickel incorporation into hydrogenases. Adv. Inorg. Chem. 11:173-192.
32. McPherson, M. J., P. Quirke, and G. R. Taylor. 1992. PCR - a practical approach. Oxford University Press, New York, N.Y.
33. Meyer, T. E., R. G. Bartsch, and M. A. Cusanovich. 1991. Adduct formation between sulfite and the flavin of phototrophic bacterial flavocytochromes c. Kinetics of sequential bleach, recolor, and rebleach of flavin as a function of pH. Biochemistry 30:8840-8845.
34. Mittenhuber, G., K. Sonomoto, M. Egert, and C. G. Friedrich. 1991. Identification of the DNA region responsible for sulfur-oxidizing ability of Thiosphaera pantotropha. J. Bacteriol. 173:7340-7344.
35. Miyazaki, J., M. Juricek, K. Angelis, K. M. Schnorr, A. Kleinhofs, and R. L. Warner. 1991. Characterization and sequence of a novel nitrate reductase from barley. Mol. Gen. Genet. 228:329-334.
36. Morgan, W. T., C. P. Hensley, and J. P. Riehm. 1972. Proteins of the thermophilic fungus Humicola lanuginosa. Isolation and aminoacid sequence of a cytochrome c. J. Biol. Chem. 247:6555-6565.
37. Nunn, D. N., and M. E. Lidstrom. 1986. Isolation and complementation analysis of 10 methanol oxidation mutant classes and identification of the methanol dehydrogenase structural gene of Methylobacterium sp. strain AM1. J. Bacteriol. 166:591-597.
38. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444-2448.
39. Pieterse, C. M., J. van't Klooster, G. C. van den Berg-Velthuis, and F. Govers. 1995. NiaA, the structural nitrate reductase gene of Phytophthora infestans: isolation, characterization and expression analysis in Aspergillus nidulans. Curr. Genet. 27:359-366.
40. Rao, M. J. K., and P. Argos. 1986. A conformational preference parameter to predict helices in integral membrane proteins. Biochim. Biophys. Acta 869:197-214.
41. Robertson, L. A., and J. G. Kuenen. 1983. Thiosphaera pantotropha gen. nov. sp. nov., a facultatively anaerobic, facultative autotrophic sulphur bacterium. J. Gen. Microbiol. 129:2847-2855.
42. Russell, P. R., and B. D. Hall. 1982. Structure of the Schizosaccharomyces pombe cytochrome c gene. Mol. Cell. Biol. 2:106-116.
43. Sambrook, J., T. Maniatis, and E. F. Fritsch. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
44. Samyn, B., B. C. Berks, M. D. Page, S. J. Ferguson, and J. J. van Beeumen. 1994. Characterization and amino acid sequence of cytochrome c-550 from Thiosphaera pantotropha. Eur. J. Biochem. 219:585-594.
45. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
46. Schneider, A., and C. G. Friedrich. 1994. Sulfide dehydrogenase is identical with the SoxB protein of the thiosulfate-oxidizing enzyme system of Paracoccus denitrificans GB17. FEBS Lett. 350:61-65.
47. Simon, R., U. Priefer, and A. Pühler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio/Technology 1:784-790.
48. Steinrücke, P., and B. Ludwig. 1993. Genetics of Paracoccus denitrificans. FEMS Microbiol. Rev. 104:83-118.
49. Toghrol, F., and W. M. Sutherland. 1983. Purification of Thiobacillus novellus sulfite oxidase. Evidence for the presence of heme and molybdenum. J. Biol. Chem. 258:6762-6766.
50. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
51. 552 and sequence analysis of the gene. Eur. J. Biochem. 231:259-265.
52. Van Beeumen, J., P. Tempst, P. Stevens, D. Bral, J. Van Damme, and J. De Ley. 1980. Cytochromes c of two different sequence classes in Agrobacterium tumefaciens. Protides Biol. Fluids Proc. Colloq. 28:69-74.
53. Visser, J. M., G. A. H. de Jong, L. A. Robertson, J. G. Kuenen. 1997. A novel membrane-bound flavocytochrome c sulfide dehydrogenase from the colorless sulfur bacterium Thiobacillus sp. W5. Arch. Microbiol. 167:295-301.
54. von Heijne, G. 1985. Signal sequences. The limits of variation. J. Mol. Biol. 184:99-105.
55. von Heijne, G. 1988. Transcending the impenetrable: how proteins come to terms with membranes. Biochim. Biophys. Acta 947:307-333.
56. Wodara, C., S. Kostka, M. Egert, D. P. Kelly, and C. G. Friedrich. 1994. Identification and sequence analysis of the soxB gene essential for sulfur oxidation of Paracoccus denitrificans GB17. J. Bacteriol. 176:6188-6191.
57. Yamanaka, T., T. Nagano, K. Shoji, and Y. Fukumori. 1991. Cytochromes c of Nitrobacter winogradskyi and Thiobacillus novellus: structure, function and evolution. Biochim. Biophys. Acta 1058:48-51.
58. Yamanaka, T., T. Yoshioka, and K. Kimura. 1981. Purification of sulphite: cytochrome c reductase of Thiobacillus novellus and the reconstitution of its sulphite oxidase system with the purified constituents. Plant Cell Physiol. 22:613-622.
59. 2O reductase and cytochrome-c oxidase. Eur. J, Biochem. 208:31-40.