1887

Abstract

The sequence of the dsr gene region of the phototrophic sulfur bacterium Chromatium vinosum D (DSMZ 180) was determined to clarify the in vivo role of ‘reverse’ sirohaem sulfite reductase. The dsrAB genes encoding dissimilatory sulfite reductase are part of a gene cluster, dsrABEFHCMK, that encodes four small, soluble proteins (DsrE, DsrF, DsrH and DsrC), a transmembrane protein (DsrM) with similarity to haem-b-binding polypeptides and a soluble protein (DsrK) resembling [4Fe---4S]-cluster-containing heterodisulfide reductase from methanogenic archaea. Northern hybridizations showed that expression of the dsr genes is increased by the presence of reduced sulfur compounds. The dsr genes are not only transcribed from a putative promoter upstream of dsrA but primary transcripts originating from (a) transcription start site(s) downstream of dsrB are also formed. Polar insertion mutations immediately upstream of dsrA, and in dsrB, dsrH and dsrM, led to an inability of the cells to oxidize intracellularly stored sulfur. The capability of the mutants to oxidize sulfide, thiosulfate and sulfite under photolithoautotrophic conditions was unaltered. Photoorganoheterotrophic growth was also unaffected. ‘Reverse’ sulfite reductase and DsrEFHCMK are, therefore, not essential for oxidation of sulfide or thiosulfate, but are obligatory for sulfur oxidation. These results, together with the finding that the sulfur globules of C. vinosum are located in the extracytoplasmic space whilst the dsr gene products appear to be either cytoplasmic or membrane-bound led to the proposal of new models for the pathway of sulfur oxidation in this phototrophic sulfur bacterium.

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1998-07-01
2024-12-07
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References

  1. Albracht S. P. J. 1994; Nickel hydrogenases: in search of the active site.. Biochim Biophys Acta 1188:167–204
    [Google Scholar]
  2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. 1997; Gapped BLAST and Psi-BLAST: a new generation of protein database search programs.. Nucleic Acids Res 25:3389–3402
    [Google Scholar]
  3. Arendsen A.F., Verhagen M.F.J.M., Wolbert A.F., Pierik A.J., Stams A.J.M., Jetten M.S.M., Hagen W.R. 1993; The dissimilatory sulfite reductase from Desulfosarcina variabilis is a desulforubidin containing uncoupled metalated sirohemes and S = 9/2 iron-sulfur clusters.. Biochemistry 32:10323–10330
    [Google Scholar]
  4. Ausubel F.A., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. 1997 Current Protocols in Molecular Biology New York: John Wiley;
    [Google Scholar]
  5. Bartsch R.G., Newton G.L., Sherrill C., Fahey R.C. 1996; Glutathione amide and its perthiol in anaerobic sulfur bacteria.. J Bacteriol 178:4742–4746
    [Google Scholar]
  6. Bazaral M., Helinski D.R. 1968; Circular DNA forms of colicinogenic factors El, E2 and E3 from Escherichia coli. . J Mol Biol 36:185–194
    [Google Scholar]
  7. Berks B.C., Page M.D., Richardson D.J., Reilly A., Cavill A., Outen F., Ferguson S.J. 1995; Sequence analysis of subunits of the membrane-bound nitrate reductase from a denitrifying bacterium: the integral membrane subunit provides a prototype for the dihaem electron-carrying arm of a redox loop.. Mol Microbiol 15:319–331
    [Google Scholar]
  8. Bobik T.A., Wolfe R.S. 1988; Physiological importance of the heterodisulfide of coenzyme M and 7-mercaptoheptanoyl- threonine phosphate in the reduction of carbon dioxide to methane in Methanobacterium. . Proc Natl Acad Sci USA 8560–63
    [Google Scholar]
  9. Brune D.C. 1989; Sulfur oxidation by phototrophic bacteria.. Biochim Biophys Acta 975:189–221
    [Google Scholar]
  10. Brune D.C. 1995a; Sulfur compounds as photosynthetic elec¬tron donors.. In Anoxygenic Photosynthetic Bacteria pp. 847–870 Edited by Blankenship R. E., Madigan M. T., Bauer E. Dordrecht: Kluwer;
    [Google Scholar]
  11. Brune D.C. 1995b; Isolation and characterization of sulfur globule proteins from Chromatium vinosum and Thiocapsa roseopersicina. . Arch Microbiol 163:391–399
    [Google Scholar]
  12. Bult C.J., White 0., Olsen G.J. 37 other authors 1996; Complete genome sequence of the methanogenic archaeon,Methanococcus jannaschii. . Science 273:1058–1073
    [Google Scholar]
  13. Chen Z.W., Koh M., van Driessche G., van Beeumen J.J., Bartsch R.G., Meyer T.E., Cusanovich M.A., Mathews F.S. 1994; The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium.. Science 266:430–432
    [Google Scholar]
  14. Cohen G., Yanko M., Mislovati M., Argaman A., Schreiber R., Av-Gay Y., Aharonowitz Y. 1993; Thioredoxin-thioredoxin reductase system of Streptomyces clavuligerus: sequences, expression and organization of the genes.. J Bacteriol 175:5159–5167
    [Google Scholar]
  15. Craske A.L., Ferguson S.J. 1986; The respiratory nitrate reductase of Paracoccus denitrificans. Molecular characterization and kinetic properties.. Eur J Biochem 158:429–436
    [Google Scholar]
  16. Dahl C. 1996; Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum. . Microbiology 142:3363–3372
    [Google Scholar]
  17. Dahl C., Trüper H.G. 1994; Enzymes of dissimilatory sulfide oxidation in phototrophic bacteria.. Methods Enzymol 243:400–421
    [Google Scholar]
  18. Dahl C., Kredich N.M., Deutzmann R., Trüper H.G. 1993; Dissimilatory sulphite reductase from Archaeoglobus fulgidus-. physico-chemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes.. J Gen Microbiol 139:1817–1828
    [Google Scholar]
  19. Dahl C., Speich N., Trüper H.G. 1994; Enzymology and molecular biology of sulfate reduction in the extremely thermo¬philic archaeon Archaeoglobus fulgidus. . Methods Enzymol 243:331–349
    [Google Scholar]
  20. Dayhoff M.O., Schwartz R.M., Orcutt B.C. 1978; A model of evolutionary change in proteins.. In Atlas of Protein Sequence and Structure pp. 345–352 Edited by Dayhoff M. O. Washington, DC: National Biochemical Research Foundation;
    [Google Scholar]
  21. Dietrichs D., Meyer M., Rieth M., Andreesen J.R. 1991; Interaction of selenoprotein PA and the thioredoxin system, components of the NADPH-dependent reduction of glycine in Eubacterium acidaminophilum and Clostridium litoralis. . J Bac-terial 173:5983–5991
    [Google Scholar]
  22. Dolata M.M., van Beeumen J.J., Ambler R.P., Meyer T.E., Cusanovich M.A. 1993; Nucleotide sequence of the heme subunit of flavocytochrome c from the purple phototrophic bacterium, Chromatium vinosum. A 2-6 kilobase pair DNA fragment contains two multiheme cytochromes, a flavoprotein, and a homolog of human ankyrin.. J Biol Chern 268:14426–14431
    [Google Scholar]
  23. Ehretsmann CP., Carpousis A.J., Krisch H.M. 1992; Specificity of Escherichia coli endoribonuclease E: in vivo and in vitro analysis of mutants in a bacteriophage T4 mRNA processing site.. Genes Dev 6:149–159
    [Google Scholar]
  24. Fellay R., Frey J., Krisch H.M. 1987; Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vivo insertional mutagenesis of Gram-negative bacteria.. Gene 52:147–154
    [Google Scholar]
  25. Fischer U. 1989; Enzymatic steps in dissimilatory sulfur metabolism by whole cells of anoxyphotobacteria.. In Biogenic Sulfur in the Environment pp. 262–279 Edited by Saltzman E., Cooper W. Washington, DC: American Chemical Society;
    [Google Scholar]
  26. George D.G., Barker W.C., Hunt L.T. 1990; Mutation data matrix and its uses.. Methods Enzymol 183:333–351
    [Google Scholar]
  27. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids.. J Mol Biol 166:557–580
    [Google Scholar]
  28. Hedderich R., Koch J., Linder D., Thauer R.K. 1994; The heterodisulfide reductase from Methanobacterium thermoauto- trophicum contains sequence motifs characteristic of pyridinenucleotide-dependent thioredoxin reductases.. Eur J Biochem 225:253–261
    [Google Scholar]
  29. Higgins D.G., Sharp P.M. 1989; clustal: a package for performing multiple sequence alignment on a microcomputer.. Gene 73:237–244
    [Google Scholar]
  30. Hipp W.M., Pott A.S., Thum-Schmitz N., Faath I., Dahl C., Trüper H.G. 1997; Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfuroxidizing prokaryotes.. Microbiology 143:2891–2902
    [Google Scholar]
  31. Hofman K., Stoffel W. 1993; TMbase-a database of membrane spanning protein segments.. Biol Chern Hoppe-Seyler 347:166–171
    [Google Scholar]
  32. Hurlbert R.E. 1968; Effect of thiol-binding reagents on the metabolism of Chromatium vinosum D.. J Bacterial 95:1706–1712
    [Google Scholar]
  33. Jacquot J.P., Rivera-Madrid R., Marinho P., Kollarova M., Le Marechal P., Miginiac-Maslow M., Meyer Y. 1994; Arabi- dopsis thaliana NADPH thioredoxin reductase cDNA characterization and expression of the recombinant protein in Escherichia coli. . J Mol Biol 235:1357–1363
    [Google Scholar]
  34. Karkhoff-Schweizer R.R., Bruschi M., Voordouw G. 1993; Expression of the γ-subunit gene of desulfoviridin-type dissimilatory sulfite reductase and of the α- and β-subunit genes is not coordinately regulated.. Eur J Biochem 211:501–507
    [Google Scholar]
  35. Klenk H.-P., Clayton R.A., Tomb J.-F. 48 other authors 1997; The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. . Nature 390:364–370
    [Google Scholar]
  36. Künkel A., Vaupel M., Heim S., Thauer R.K., Hedderich R. 1997; Heterodisulfide reductase from methanol-grown cells of Methanosarcina barkeri is not a flavoenzyme.. Eur J Biochem 244:226–234
    [Google Scholar]
  37. Lisser S., Margalit H. 1993; Compilation of E. coli mRNA promoter sequences.. Nucleic Acids Res 21:1507–1516
    [Google Scholar]
  38. Lübbers M., Andreesen J.R. 1993; Components of glycine reductase from Eubacterium acidaminophilum. Cloning, sequencing and identification of the genes for thioredoxin reductase, thioredoxin and selenoprotein PA.. Eur J Biochem 217:791–798
    [Google Scholar]
  39. Molitor M., Dahl C., Molitor I., Schäfer U., Speich N., Huber R., Deutzmann R., Trüper H.G. 1998; A dissimilatory sirohaem- sulfite reductase-type protein from the hyperthermophilic archaeon Pyrobaculum islandicum. . Microbiology 144:529–541
    [Google Scholar]
  40. Pattaragulwanit K., Dahl C. 1995; Development of a genetic system for a purple sulfur bacterium: conjugative plasmid transfer in Chromatium vinosum. . Arch Microbiol 164:217–222
    [Google Scholar]
  41. Pattaragulwanit K., Brune D.C, Trüper H.G., Dahl C. 1998; Molecular genetic evidence for extracytoplasmic localization of sulfur globules in Chromatium vinosum. . Arch Microbiol in press
    [Google Scholar]
  42. Pfennig N., Trüper H.G. 1989; Anoxygenic phototrophic bacteria.. In Bergey’s Manual of Systematic Bacteriology 3 pp. 1635–1653 Edited by Staley J. T., Bryant M. P., Pfennig N., Holt J. G. Baltimore: Williams & Wilkins;
    [Google Scholar]
  43. Pierik A.J., Duyvis M.G., van Helvoort J.M.L.M., Wolbert R.B.G., Hagen W.R. 1992; The third subunit of desulfoviridin-type dissimilatory sulfite reductases.. Eur J Biochem 205:111–115
    [Google Scholar]
  44. Rakhely G., Colbeau A., Garin J., Vignais P.N., Kovdás K.L. 1998; Unusual gene organization of HydSL, the stable [NiFe]hydrogenase in the photosynthetic bacterium Thiocapsa roseopersicina. . J Bacterial 180:1460–1465
    [Google Scholar]
  45. Reynolds R., Bermudez-Cruz R.M., Chamberlin M.J. 1992; Parameters affecting transcription termination by Escherichia coli RNA. I. Analysis of 13 rho-independent terminators.. J Mol Biol 224:31–51
    [Google Scholar]
  46. Rossi M., Pollock B.R., Reiji M.W., Keon R.G., Fu R., Voordouw G. 1993; The hmc operon of Desulfovibrio vulgaris subsp.vulgaris Hildenborough encodes a potential transmembrane redox protein complex.. J Bacteriol 175:4699–4711
    [Google Scholar]
  47. Russel M., Model P. 1988; Sequence of thioredoxin reductase from Escherichia coli. Relationship to other flavoprotein disulfide oxidoreductases.. J Biol Chern 263:9015–9019
    [Google Scholar]
  48. Sambrook J., Fritsch E.F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  49. Schedel M., Vanselow M., Trüper H.G. 1979; Siroheme sulfite reductase from Chromatium vinosum. Purification and investigation of some of its molecular and catalytic properties.. Arch Microbiol 121:29–36
    [Google Scholar]
  50. Simon R., Priefer U., Pühler A. 1983; A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria.. Bio /Technology 1:784–791
    [Google Scholar]
  51. Smith A.J. 1966; The role of tetrathionate in the oxidation of thiosulphate by Chromatium sp. strain D.. J Gen Microbiol 42:371–380
    [Google Scholar]
  52. Steuber J., Arendsen A.F., Hagen W.R., Kroneck P.M.H. 1995; Molecular properties of the dissimilatory sulfite reductase from Desulfovibrio desulfuricans (Essex) and comparison with the enzyme from Desulfovibrio vulgaris (Hildenborough).. Eur J Biochem 233:873–879
    [Google Scholar]
  53. Trüper H.G. 1984; Phototrophic bacteria and their sulfur metabolism.. In Sulfur, its Significance for Chemistry, for the Geo-, Bio-, and Cosmosphere and Technology pp. 367–382 Edited by Muller A., Krebs B. Amsterdam: Elsevier;
    [Google Scholar]
  54. Trüper H.G., Fischer U. 1982; Anaerobic oxidation of sulphur compounds as electron donors for bacterial photosynthesis.. Philos Trans R Soc Lond Ser B Biol Sci 298:529–542
    [Google Scholar]
  55. Voordouw G. 1995; The genus Desulfovibrio: the centennial.. Appl Environ Microbiol 61:2813–2819
    [Google Scholar]
  56. Weaver P.F., Wall J.D., Gest H. 1975; Characterization of Rhodopseudomonas capsulata. . Arch Microbiol 105:207–216
    [Google Scholar]
  57. Wilkinson M. 1991; Purification of RNA.. In Essential Molecular Biology 1 pp. 69–87 Edited by Brown T. A. Oxford: Oxford University Press;
    [Google Scholar]
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