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Volume 139, Issue 8

Dissimilatory sulphite reductase from : physico-chemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes Free

Abstract

SUMMARY: A dissimilatory sulphite reductase was isolated from the extremely thermophilic dissimilatory sulphate-reducing archaeon In common with other dissimilatory sulphite reductases thus far characterized, the enzyme has an αβ-structure and contains sirohaem, non-haem iron atoms and acid labile sulphide. The oxidized enzyme exhibited absorption maxima at 281, 394, 545 and 593 nm with a weak band around 715 nm. We have cloned and sequenced the genes for the α and β subunits of this enzyme, which we designate and respectively. They are contiguous in the order and probably comprise an operon, since is preceded by sequences characteristic of promoters in methanogenic archaea, and is followed by a sequence resembling termination signals in extremely thermophilic sulphur-dependent archaea. and encode 47.4 kDa and 41.7 kDa peptides, which have 25.6% amino acid sequence identity, indicating that they may have arisen by duplication of an ancestral gene. Each deduced peptide contains cysteine clusters resembling those postulated to bind sirohaem-[FeS] complexes in sulphite reductases and nitrite reductases from other species. The encoded peptide lacks a single cysteine residue in one of the two clusters, suggesting that only the α subunit binds a sirohaem-[FeS] complex, and chemical analyses showed the presence of only two sirohaems per αβ enzyme molecule. Both deduced peptides also contain an arrangement of cysteine residues characteristic of [FeS] ferredoxins, and chemical analyses were consistent with the presence of six [FeS] clusters per αβ enzyme molecule, two of which would be expected to be associated with sirohaem while the other four could bind to the ferredoxin-like sites.

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© Society for General Microbiology, 1993
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1993-08-01
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References

  1. Achenbach-Richter L., Stetter K.O., Woese C.R. 1987; A possible biochemical missing link among archaebacteria.. Nature; London : 327348–349
     [Google Scholar]
  2. Adman E.T., Sieker L.C., Jensen L.H. 1973; The structure of a bacterial ferredoxin.. Journal of Biological Chemistry 248:3987–3996
     [Google Scholar]
  3. Adman E.T., Sieker L.C., Jensen L.H. 1976; Structure ofPeptococcus aerogenesferredoxin: refinement at 2Å resolution.. Journal of Biological Chemistry 251:3801–3808
     [Google Scholar]
  4. Amesz J., Knaff D.B. 1988; Molecular mechanisms of bacterial photosynthesis.. In Biology of Anaerobic Microorganisms pp. 113–178 Zehnder A.J.B. Edited by New York: John Wiley & Sons;
     [Google Scholar]
  5. Back E., Burkhart W., Moyer M., Privalle L., Rothstein S. 1988; Isolation of cDNA clones coding for spinach nitrate reductase: complete sequence and nitrate induction.. Molecular and General Genetics 212:20–26
     [Google Scholar]
  6. Brown J.W., Daniels C.J., Reeve J.N. 1989; Gene structure, organization, and expression in archaebacteria.. Critical Reviews in Microbiology 16:287–338
     [Google Scholar]
  7. Bruschi M., Hatchikian E.C. 1982; Non-heme iron proteins ofDesulfovibrio: the primary structure of ferredoxin I fromD.africanus. . Biochimie 64:503–507
     [Google Scholar]
  8. Bruschi M., Guerlesquin F. 1988; Structure, function and evolution of bacterial ferredoxins.. FEMS Microbiology Reviews 54:155–176
     [Google Scholar]
  9. Burggraf S., Jannasch H.W., Nicolaus B., Stetter K.O. 1990; Archaeoglobus profundussp.nov., represents a new species within the sulfate-reducing archaebacteria.. Systematic and Applied Microbiology 13:24–28
     [Google Scholar]
  10. Chisholm D. 1989; A convenient moderate-scale procedure for obtaining DNA from bacteriophage lambda.. Biofeedback 7:21–23
     [Google Scholar]
  11. Cram D.S., Sherf A., Libby R.T., Mattaliano R.J., Ramachandran K.L., Reeve J.N. 1987; Structure and expression of the genes,mcrBDCGA,which encode the subunits of component C of methyl coenzyme M reductase inMethanococcus vannielii. . Proceedings of the National Academy of Sciences of the United States of America 84:3992–3996
     [Google Scholar]
  12. Cue D., Beckler G.S., Reeve J.N., Konisky J. 1985; Structure and sequence divergence of two archaebacterial genes.. Proceedings of the National Academy of Sciences of the United States of America 82:4207–4211
     [Google Scholar]
  13. Dahl C., Koch H.G., Keuken O., TrÜper H.G. 1990; Purification and characterization of ATP sulfurylase from the extremely thermophilic archaebacterial sulfate-reducer,Archaeoglobus fulgidus. . FEMS Microbiology Letters 67:27–32
     [Google Scholar]
  14. Dayhoff M.O., Schwartz R.M., Orcutt B.C. 1978; A model of evolutionary change in proteins.. In Atlas of Protein Sequence and Structure 5 suppl.3 pp. 345–352 Dayhoff M.O. Washington, DC: National Biomedical Research Foundation.;
     [Google Scholar]
  15. Devereux J., Haeberli P., Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX.. Nucleic Acids Research 12:387–395
     [Google Scholar]
  16. Devereux R., Delaney M., Widdel F., Stahl D.A. 1989; Natural relationships among sulfate-reducing eubacteria.. Journal of Bacteriology 171:6689–6695
     [Google Scholar]
  17. Drake H.L., Akagi J.M. 1977; Bisulfite reductase ofDesulfovibrio vulgaris :explanation for product formation.. Journal of Bacteriology 132:139–143
     [Google Scholar]
  18. Fauque G., Lino A.R., Czechowski M., Kang L., Der Vartanian D.V., Moura J.J.G., Legall J., Moura I. 1990; Purification and characterization of bisulfite reductase (desulfo-fuscidin) fromDesulfovibrio thermophilusand its complexes with exogenous ligands.. Biochimica et Biophysica Acta 1040:112–118
     [Google Scholar]
  19. Fauque G., Legall J., Barton L. 1991; Sulfate-reducing and sulfur-reducing bacteria.. In Variations in Autotrophic Life pp. 271–337 Shively J.M., Barton L. Edited by New York: Academic Press.;
     [Google Scholar]
  20. Feinberg A.P., Vogelstein B. 1983; A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.. Analytical Biochemistry 132:6–13
     [Google Scholar]
  21. Ferguson S.J., Jackson J.B., Mcewan A.G. 1987; Anaerobic respiration in the Rhodospirillaceae: characterisation of pathways and evaluation of roles in redox balancing during photosynthesis.. FEMS Microbiology Reviews 46:117–143
     [Google Scholar]
  22. George D.H., Hunt L.T., Yeh L.S.L., Barker W.C. 1985; New perspectives on bacterial ferredoxin evolution.. Journal of Molecular Evolution 22:20–31
     [Google Scholar]
  23. Gribskov M., Burgess R.R. 1986; Sigma factors fromE.Coli B.subtilis,phage SPOl, and phage T4 are homologous proteins.. Nucleic Acids Research 14:6745–6763
     [Google Scholar]
  24. Hase T., Ohmiya N., Matsubara H., Mullinger R.N., Rao K.K., Hall D.O. 1976; Amino acid sequence of a four-iron-four- sulfur ferredoxin from Bacillus stearothermophilus. . Biochemical Journal 159:55–63
     [Google Scholar]
  25. Hatchikian E.C., Zeikus J.G. 1983; Characterization of a new type of dissimilatory sulfite reductase present inThermodesulfo-bacterium commune. . Journal of Bacteriology 153:1211–1220
     [Google Scholar]
  26. Hausner W., Frey G., Thomm M. 1991; Control regions of AN archaeal gene.A TATA Box and an initiator element promote cell free transcription of the tRNA Val gene ofMethanococcus vannielii. . Journal of Molecular Biology 222:495–508
     [Google Scholar]
  27. Huang C.J., Barrett E.L. 1991; Sequence analysis and expression of theSalmonella typhimurium asroperon encoding production of hydrogen sulfide from sulfite.. Journal of Bacteriology 173:1544–1553
     [Google Scholar]
  28. Hucklesby D.P., James D.M., Banwell M.J., Hewitt E.J. 1976; Properties of nitrite reductase fromCucurbita pepo. . Phyto-chemistry 15:599–603
     [Google Scholar]
  29. Huynh B.H., Kang L., Der Vartanian D.V., Peck H.D.JR., Legall J. 1984; Characterization of a sulfite reductase fromDesulfovibrio vulgaris.Evidence for the presence of a low-spin siroheme and an exchange-coupled siroheme-[4Fe-4S] unit.. Journal of Biological Chemistry 259:15373–15376
     [Google Scholar]
  30. Jackson R.H., Cornish-Bowden A., Cole J.A. 1981; Prosthetic groups of the NADH-dependent nitrite reductase fromEscherichia coliK12.. Biochemical Journal 193:861–867
     [Google Scholar]
  31. King T.E., Morris R.O. 1966; Determination of acid-labile sulfide and sulfhydryl groups.. Methods in Enzymology 10:635–641
     [Google Scholar]
  32. Kinghorn J.R., Campbell E.I. 1989; Amino acid sequence relationships between bacterial, fungal, and plant nitrate and nitrite reductase proteins.. In Molecular and Genetic Aspects of Nitrate Assimilation, pp. 385–403 Wray J.L., Kinghorn J.R. Edited by Oxford: Oxford Science Publications;
     [Google Scholar]
  33. Kyte J., Doolittle R.F. 1982; A simple method for displaying the hydropathic character of a protein.. Journal of Molecular Biology 157:105–132
     [Google Scholar]
  34. Lampreia J., Fauque G., Speich N., Dahl C., Moura I., Truper H.G., Moura J.J.G. 1991; Spectroscopic studies on APS reductase isolated from the hyperthermophilic sulfate-reducing archaebacteriumArchaeoglobus fulgidus. . Biochemical and Biophysical Research Communications 181:342–347
     [Google Scholar]
  35. Lee J.-P., Peck H.D. JR. 1971; Purification of the enzyme reducing bisulfite to trithionate fromDesulfovibrio gigasand its identification as desulfoviridin.. Biochemical and Biophysical Research Communications 45:583–589
     [Google Scholar]
  36. Lee J.-P., Yi C.-S., Legall J., Peck H.D. JR. 1973; Isolation of a new pigment, desulforubidin, fromDesulfovibrio desulfuriccms(Norway strain) and its role in sulfite reduction.. Journal of Bacteriology 115:453–455
     [Google Scholar]
  37. Legall J., Fauque G. 1988; Dissimilatory reduction OF sulfur compounds.. In Biology of Anaerobic Microorganisms pp. 587–639 Zehnder A.J.B. Edited by New York: J.Wiley & Sons.;
     [Google Scholar]
  38. Massey V. 1957; Studies on succinic dehydrogenase.VII.Valency state ofthe iron in beef heart dehydrogenase.. Journal of Biological Chemistry 229:763–770
     [Google Scholar]
  39. Mead D.A., Szczesna-Skorupa E., Kemper B. 1986; Singlestranded DNA “blue” T7 promoter plasmids: a versatile tandem promoter system for cloning and protein engineering.. Protein Engineering 1:67–74
     [Google Scholar]
  40. Miller J.H. 1972 Experiments in Molecular Genetics pp. 431–433 Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;
     [Google Scholar]
  41. Moura I., Lino A.R., Moura J.J.G., Xavier A.V., Fauque G., Peck H.D. JR Legall J. 1986; Low-spin sulfite reductases: a new homologous group of non-heme iron-siroheme proteins in anaerobic bacteria.. Biochemical and Biophysical Research Communications 141:1032–1041
     [Google Scholar]
  42. Moura I., Legall J., Lino A.R., Peck H.D. JR. Fauque G., Xavier A.V., Der Vartanian D.V., Moura J.J.G., Huynh B.H. 1988; Characterization of two dissimilatory sulfite reductases (desulforubidin and desulfoviridin) from the sulfate-reducing bacteria.Mössbauer and EPR studies.. Journal of the American Chemical Society 110:1075–1082
     [Google Scholar]
  43. Murphy M.J., Siegel L.M. 1973; Siroheme and sirohydro- chlorin: the basis for a new type of porphyrin-related prosthetic group common to both assimilatory and dissimilatory sulfite reductases.. Journal of Biological Chemistry 248:6911–6919
     [Google Scholar]
  44. Murphy M.J., Siegel L.M., Kamin H., Rosenthal D. 1973; Reduced nicotinamide adenine dinucleotide phosphate-sulfite reductase of enterobacteriaceae.II.Identification of a new class of heme prosthetic group: an iron-tetrahydroporphyrin (isobacterio-chlorin type) with eight carboxylic groups.. Journal of Biological Chemistry 248:2801–2814
     [Google Scholar]
  45. Ostrowski J., Barber M.J., Rueger D.C., Miller B.E., Siegel L.M., Kredich N.M. 1989a; Characterization of the flavoprotein moieties of NADPH-sulfite reductase fromSalmonella typhimuriumandEscherichia coli: physicochemical and catalytic properties, amino acid sequence deduced from the DNA sequence ofcysJand comparison with NADPH-cytochrome P-450 reductase.. Journal of Biological Chemistry 264:15796–15808
     [Google Scholar]
  46. Ostrowski J., Wu J.-Y., Rueger D.C., Miller B.E., Siegel L.M., Kredich N.M. 1989b; Characterization of thecysJIHregions ofSalmonella typhimuriumandEscherichia coliB: DNA sequences ofcyslandcysHand a model for the siroheme-Fe4S4active center of sulfite reductase hemoprotein based on amino acid homology with spinach nitrite reductase.. Journal of Biological Chemistry 264:15726–15737
     [Google Scholar]
  47. Peakman T., Crouzet J., Mayaux J.F., Busby S., Mohan S., Harborne N., Wootton J., Nicolson R., Cole J. 1990; Nucleotide sequence, organisation and structural analysis of the products of genes in thenirB-cysGregion of theEscherichia coliK12 chromosome.. European Journal of Biochemistry 191:315–323
     [Google Scholar]
  48. Peck H.D. JR. 1962; Comparative metabolism of inorganic sulfur compounds in microorganisms.. Bacteriological Reviews 26:67–94
     [Google Scholar]
  49. Peck H.D. JR. Legall J. 1982; Biochemistry of dissimilatory sulphate reduction.. Philosophical Transactions of the Royal Society London 298B:443–466
     [Google Scholar]
  50. Peck H.D. JR. Lissolo T. 1988; Assimilatory and dissimilatory sulfate reduction: enzymology and bioenergetics.. Symposia of the Society for General Microbiology 42:98–132
     [Google Scholar]
  51. 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 reductase.. European Journal of Biochemistry 205:111–115
     [Google Scholar]
  52. Reeve J.N., Hamilton P.T., Beckler G.S., Morris C.J., Clarke C.H. 1986; Structure of methanogen genes.. Systematic and Applied Microbiology 7:5–10
     [Google Scholar]
  53. Reiter W.D., Palm P., Zillig W. 1988; Transcription termination in the archaebacteriumSulfolobus:signal structures and linkage to transcription initiation.. Nucleic Acids Research 16:2445–2459
     [Google Scholar]
  54. Rozanova E.P., Pivovarova T.A. 1988; Reclassification ofDesulfovibrio thermophilus(Rozanova, Khudyakova, 1974).. Mikrobiologiya 57:102–106
     [Google Scholar]
  55. 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]
  56. Sanger F., Nicklen S., Coulson A.R. 1977; DNA sequencing with chain-terminating inhibitors.. Proceedings of the National Academy of Sciences of the United States of America 74:5463–5467
     [Google Scholar]
  57. Sargent T.D. 1987; Isolation of differentially expressed genes.. Methods in Enzymology 152:423–432
     [Google Scholar]
  58. Schedel M., Legall J., Baldensperger J. 1975; Sulfur metabolism in Thiobacillus denitrificans.Evidence for the presence of a sulfite reductase activity.. Archives of Microbiology 105:339–341
     [Google Scholar]
  59. Schedel M., Vanselow M., TrÜper H.G. 1979; Siroheme-sulfite reductase isolated fromChromatium vinosum.Purification and investigation of some of its molecular and catalytic properties.. Archives of Microbiology 121:29–36
     [Google Scholar]
  60. Schwartz R.M., Dayhoff M.O. 1978; Matrices for detecting distant relationships.. In Atlas of Protein Sequence and Structure 5 suppl.3 pp. 353–358 Dayhoff M.O. Edited by Washington, DC: National Biomedical Research Foundation.;
     [Google Scholar]
  61. Siegel L.M., Murphy M.J., Kamin H. 1978; Siroheme: methods of isolation and characterization.. Methods in Enzymology 52:436–447
     [Google Scholar]
  62. Speich N. 1991; Enzymologische und molekularbiologische Charakterisierung der Adenosin-5ʹ-Phosphosulfat-Reduktase aus Archaeoglobus fulgidus.. PhD thesis University Of Bonn; Germany.:
     [Google Scholar]
  63. Speich N., TrÜper H.G. 1988; Adenylylsulphate reductase in a dissimilatory sulphate-reducing archaebacterium.. Journal of General Microbiology 134:1419–1425
     [Google Scholar]
  64. Stetter K.O. 1988; Archaeoglobus fulgidusgen.nov., sp.nov.: a new taxon of extremely thermophilic archaebacteria.. Systematic and Applied Microbiology 10:172–173
     [Google Scholar]
  65. Stetter K.O., Lauerer G., Thomm M., Neuner A. 1987; Isolation of extremely thermophilic sulfate reducers: evidence for a/ novel branch of archaebacteria.. Science 236:822–824
     [Google Scholar]
  66. Stolzenberg A.M., Strauss S.H., Holm R.H. 1981; Iron(II,III)-chlorin and -isobacteriochlorin complexes.Models of the heme prosthetic groups in nitrite and sulfite reductases: means of formation and spectroscopic and redox properties.. Journal of the American Chemical Society 103:4763–4778
     [Google Scholar]
  67. Tan J., Helms L.R., Swenson R.P., Cowan J.A. 1991; Primary structure of the assimilatory-type sulfite reductase fromDesulfovibrio vulgaris(Hildenborough): cloning and nucleotide sequence of the reductase gene.. Biochemistry 30:9000–9007
     [Google Scholar]
  68. Trudinger P.A. 1970; Carbon monoxide-reacting pigment fromDesulfotomaculum nigrificansand its possible relevance to sulfite reduction.. Journal of Bacteriology 104:158–170
     [Google Scholar]
  69. Vega J.M., Kamin H. 1977; Spinach nitrite reductase.Purification and properties of a siroheme-containing iron-sulfur enzyme.. Journal of Biological Chemistry 252:896–909
     [Google Scholar]
  70. Vega J.M., Garrett R.H., Siegel L.M. 1975; Siroheme: a prosthetic group of theNeurospora crassaassimilatory nitrite reductase.. Journal of Biological Chemistry 250:7980–7989
     [Google Scholar]
  71. Weil C.F., Cram D.S., Sherf B.A., Reeve J.N. 1988; Structure and comparative analysis of the genes encoding component C of methyl coenzyme M reductase in the extremely thermophilic archaebacteriumMethanothermus fervidus. . Journal of Bacteriology 170:4718–4726
     [Google Scholar]
  72. Wich G., Hummel H., Jarsch M., Bar U., Bock A. 1988; Transcription signals for stable RNA genes inMethanococcus. . Nucleic Acids Research 14:2459–2463
     [Google Scholar]
  73. Woese C.R., Kandler O., Wheelis M.L. 1990; Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.. Proceedings of the National Academy of Sciences of the United States of America 87:4576–4579
     [Google Scholar]
  74. Woese C.R., Achenbach L., Rouviere P., Mandelco L. 1991; Archaeal phylogeny: reexamination of the phylogenetic position ofArchaeoglobus fulgidusin light of certain composition-induced artifacts.. Systematic and Applied Microbiology 14:364–371
     [Google Scholar]
  75. Zumft W.G. 1972; Ferredoxin-nitrite oxidoreductase fromChlorella: purification and properties.. Biochimica et Biophysica Acta 276:363–375
     [Google Scholar]
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Dissimilatory sulphite reductase from Archaeoglobus fulgidus: physico-chemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes
Microbiology 139, 1817 (1993); https://doi.org/10.1099/00221287-139-8-1817
/content/journal/micro/10.1099/00221287-139-8-1817
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