1887

Abstract

Summary: The genes for adenosine-5′-phosphosulfate (APS) reductase, , and sirohaem sulfite reductase, , from the sulfur-oxidizing phototrophic bacterium strain D (DSMZ 180) were cloned and sequenced. Statistically significant sequence similarities and similar physicochemical properties suggest that the and gene products from . vinosum are true homologues of their counterparts from the sulfate-reducing chemotrophic archaeon and the sulfate-reducing chemotrophic bacterium . Evidence for the proposed duplication of a common ancestor of the genes is provided. Phylogenetic analyses revealed a greater evolutionary distance between the enzymes from and than between those from and . The data reported in this study are most consistent with the concept of common ancestral protogenotic genes both for dissimilatory sirohaem sulfite reductases and for APS reductases. The gene was demonstrated to be a suitable DNA probe for the identification of genes from organisms of different phylogenetic positions. PCR primers and conditions for the amplification of homologous regions are described.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-143-9-2891
1997-09-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/143/9/mic-143-9-2891.html?itemId=/content/journal/micro/10.1099/00221287-143-9-2891&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
    [Google Scholar]
  2. Ausubel F. A., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. 1996 Current Protocols in Molecular Biology. New York: John Wiley;
    [Google Scholar]
  3. Bairoch A. 1992; prosite: a dictionary of sites and patterns in proteins. Nucleic Acids Res 20:2013–2018
    [Google Scholar]
  4. Baldensperger J., Garcia J.-L. 1975; Reduction of oxidized inorganic nitrogen compounds by a new strain of Thiobacillus denitrificans . Arch Microbiol 103:31–36
    [Google Scholar]
  5. Bazaral M., Helinski D. R. 1968; Circular DNA forms of colicinogenic factors El, E2 and E3 from Escherichia coli . J MolBiol 36:185–194
    [Google Scholar]
  6. Benachenhou-Lahfa N., Forterre P., Labedan B. 1993; Evolution of glutamate dehydrogenase genes: evidence for two paralogous protein families and unusual branching patterns of the archaebacteria in the universal tree of life. J Mol Biol 36:335–346
    [Google Scholar]
  7. Benner S. A., Ellington A. D. 1990; ‘Progenote’ or ‘ protogenote ’?. Science 248:943–944
    [Google Scholar]
  8. Benner S. A., Ellington A. D., Tauer A. 1989; Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci USA 86:7054–7058
    [Google Scholar]
  9. Bowen T. J., Happold F. C., Taylor B. F. 1966; Studies on adenosine-5ʹ-phosphosulphate reductase from Thiobacillus denitrificans . Biochim Biophys Acta 118:566–576
    [Google Scholar]
  10. Brune D. C. 1989; Sulfur oxidation by phototrophic bacteria. Biochim Biophys Acta 975:189–221
    [Google Scholar]
  11. Campbell W. H., Kinghorn J. R. 1990; Functional domains of assimilatory nitrate reductases and nitrite reductases. Trends Biochem Sci 15:315–319
    [Google Scholar]
  12. Chou Q., Russell M., Birch D. E., Raymond J., Bloch W. 1992; Prevention of pre-PCR mis-priming and primer dimerization improves low-copy-number amplification. Nucleic Acids Res 20:1717–1723
    [Google Scholar]
  13. Cohan F. M. 1996; The role of genetic exchange in bacterial evolution. ASM News 62:631–636
    [Google Scholar]
  14. Crane B. R., Siegel L. M., Getzoff E. D. 1995; Sulfite reductase structure at 1.6 Å: evolution and catalysis for reduction of inorganic anions. Science 270:59–67
    [Google Scholar]
  15. Dahl C. 1996; Insertional gene inactivation in a phototrophic sulphur bacterium:APS-reductase-deficient mutants of Chromatium vinosum . Microbiology 1423363–3372
    [Google Scholar]
  16. 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 Microbiol Lett 67:27–32
    [Google Scholar]
  17. 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]
  18. Dayhoff M. O. 1978 Atlas of Protein Sequence and Structure. Washington, DC: National Biomedical Research Foundation;
    [Google Scholar]
  19. Diaz-Lazcoz Y., Henaut A., Vigier P., Risler J.-L. 1995; Differential codon usage for conserved amino acids: evidence that the serine codons TCN were primordial. J Mol Biol 250:123–127
    [Google Scholar]
  20. Doolittle R. F. 1994; Convergent evolution: the need to be explicit. Trends Biochem Sci 19:15–18
    [Google Scholar]
  21. Fauque G., LeGall J., Barton L. 1991; Sulfate-reducing and sulfur-reducing bacteria. In Variations in Autotrophic Life pp. 271–337 Edited by Shively J. M., Barton L. New York: Academic Press;
    [Google Scholar]
  22. Felsenstein J. 1993; phylip (Phylogeny Inference Package) version 3.5c. ftp.bio.indiana.edu/molbio/evolve.
  23. Fischer U. 1989; Enzymatic steps and dissimilatory sulfur metabolism by whole cells of anoxyphotobacteria. In Biogenic Sulfur in the Environment pp. 262–279 Edited by Saltzman E. S., Cooper W. J. Washington, DC: American Chemical Society;
    [Google Scholar]
  24. Fitch W. M., Margoliash E. 1967; Construction of phylogenetic trees. Science 155:279–284
    [Google Scholar]
  25. Geourjon C., Deleage G. 1995; sopma: significant improvements in protein secondary structure prediction by prediction from multiple alignments. Comput Appl Biosci 11681–684
    [Google Scholar]
  26. Gish W., States D. 1993; Identification of protein coding regions by database similarity search. Nat Genet 3:266–272
    [Google Scholar]
  27. Gogarten J. P. 1994; Which is the most conserved group of proteins? Homology-orthology, paralogy, xenology, and the fusion of independent lineages. J Mol Biol 39:541–543
    [Google Scholar]
  28. Hatchikian E. C. 1994; Desulfofuscidin: dissimilatory, high-spin sulfite reductase of thermophilic, sulfate-reducing bacteria. Methods Enzymol 243:276–295
    [Google Scholar]
  29. Henikoff S. 1984; Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28:351–359
    [Google Scholar]
  30. Henikoff S., Henikoff J. G. 1992; Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 89:10915–10919
    [Google Scholar]
  31. Henikoff S., Henikoff J. G. 1994; Protein family classification based on searching a database of blocks. Genomics 19:97–107
    [Google Scholar]
  32. Hipp W. M. 1996 The Red Book Bulletin. Current Protocols in Molecular Biology suppl. 3, units 2 9.2–2.10. Edited by Ausubel F. A. , Brent R. , Kingston R. E. , Moore D. D. , Seidman J. G. , J. A. Smith , Struhl K. . New York: John Wiley;
    [Google Scholar]
  33. Imhoff J. F. 1992; The family Ectothiorhodospiraceae. In The Prokaryotes 2nd edn, pp. 3222–3229 Edited by Balows A., Trüper H. G., Dworkin M., Harder W., Schleifer K.-H. New York: Springer;
    [Google Scholar]
  34. Imhoff J. F., Trüper H. G. 1992; The genus Rhodospirillum and related genera. In The Prokaryotes 2nd edn, pp. 2141–2155 Edited by Balows A., Trüper H. G., Dworkin M., Harder W., Schleifer K.-H. New York: Springer;
    [Google Scholar]
  35. Iwabe N., Kuma K.-I., Hasegawa M., Osawa S., Miyata T. 1989; Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci USA 86:9355–9359
    [Google Scholar]
  36. Iwasaki T., Wakagi T., Isogai Y., Tanaka K., lizuka T., Oshima T. 1994; Functional and evolutionary implications of a [3Fe–4S] cluster of the dicluster-type ferredoxin from the thermoacidophilic archaeon, Sulfolobus sp. strain 7. J Biol Chem 269:29444–29450
    [Google Scholar]
  37. Karkhoff-Schweizer R. R., Huber D. P. W., Voordouw G. 1995; Conservation of the genes for dissimilatory sulfite reductase from Desulfovibrio vulgaris and Archaeoglobus fulgidus allows their detection by PCR. Appl Environ Microbiol 61:290–296
    [Google Scholar]
  38. Kirchhoff J., Trüper H. G. 1974; Adenylylsulfate reductase of Chlorobium limicola . Arch Microbiol 100:115–120
    [Google Scholar]
  39. Kretz K., Callen W., Hedden V. 1994; Cycle sequencing. PCR Methods Appl 3:S107–S112
    [Google Scholar]
  40. Kumar S. 1996; phyltest : a program for testing phylogenetic hypothesis, version 2.0. [email protected].
  41. Lampreia J., Moura I., Teixeira M., Peck H. D., Jr, LeGall J., Huynh B. H., Moura J. J. G. 1990; The active centers of adenylylsulfate reductase from Desulfovibrio gigas . Eur J Biochem 188:653–664
    [Google Scholar]
  42. Lampreia J., Fauque G., Speich N., Dahl C., Moura I., Trüper H., G& Moura J. J. G. 1991; Spectroscopic studies on APS reductase isolated from the hyperthermophilic sulfate-reducing archae-bacterium Archaeoglobus fulgidus . Biochem Biophys Res Commun 181:342–347
    [Google Scholar]
  43. Lampreia J., Pereira A. S., Moura J. J. G. 1994; Adenylylsulfate reductase from sulfate-reducing bacteria. Methods Enzymol 243:241–260
    [Google Scholar]
  44. Lawrence C. E., Altschul S. F., Boguski M. S., Liu J. S., Neuwald A. F., Wootton J. C. 1993; Detecting subtle sequence signals: a Gibbs sampling strategy for multiple alignment. Science 262:208–214
    [Google Scholar]
  45. Lion T., Haas O. A. 1990; Nonradioactive labeling of probe with digoxigenin by polymerase chain reaction. Anal Biochem 188:335–337
    [Google Scholar]
  46. Lockhart P. J., Steel M. A., Larkum A. W. D. 1996; Gene duplication and the evolution of photosynthetic reaction center proteins. FEBS Lett 385:193–196
    [Google Scholar]
  47. Mehta P. K., Heringa J., Argos P. 1995; A simple and fast approach to prediction of protein secondary structure from multiply aligned sequences with accuracy above 70 %. Protein Sci 4:2517–2525
    [Google Scholar]
  48. Miller J. H. 1972 Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  49. Molitor M. 1966; Molekularbiologische und physikochemische Charakterisierung der dissimilatorischen Sulfitreduktasen aus Pyrobaculum islandicum und Desulfovibrio simplex. PhD thesis University of Bonn;
    [Google Scholar]
  50. Moodie S. L., Mitchell J. B. O., Thornton J. M. 1996; Protein recognition of adenylate: an example of a fuzzy recognition template. J Mol Biol 263:486–500
    [Google Scholar]
  51. Nakamura K., Yamaki M., Sarada M., Nakayama S., Vibat C. R. T., Gennis R. B., Nakayashiki T., Inokuchi H., Kojima S., Kita K. 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
    [Google Scholar]
  52. Neutzling O., Pfleiderer C., Trüper H. G. 1985; Dissimilatory sulphur metabolism in phototrophic ‘non-sulphur’ bacteria. J Gen Microbiol 131:791–798
    [Google Scholar]
  53. Nisbet E. G., Cann J. R., van Dover C. L. 1995; Origins of photosynthesis. Nature 373:479–480
    [Google Scholar]
  54. Odom J. M., Jessie K., Knodel E., Emptage M. 1991; Immunological cross-reactivities of adenosine-5ʹ-phosphosulfate reductases from sulfate-reducing and sulfide-oxidizing bacteria. Appl Environ Microbiol 57:727–733
    [Google Scholar]
  55. Olsen G. J., Woese C. R., Overbeek R. 1994; The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol 176:1–6
    [Google Scholar]
  56. Osawa S., Jukes T. H., Watanabe K., Muto A. 1992; Recent evidence for evolution of the genetic code. Microbiol Rev 56:229–264
    [Google Scholar]
  57. Ostrowski J., Wu J.-Y., Rueger D. C., Miller B. E., Siegel, L M., Kredich N. M. 1989; Characterization of the cysJIH regions of Salmonella typhimurium and Escherichia coli B. J Biol Chem 264:15726–15737
    [Google Scholar]
  58. Pfennig N., Trüper H. G. 1992; The family Chromatiaceae. In The Prokaryotes 2nd edn, pp. 3200–3221 Edited by Balows A., Trüper H. G., Dworkin M., Harder W., Schleifer K.-H. New York: Springer;
    [Google Scholar]
  59. Richardson J. P. 1993; Transcription termination. Crit Rev Biochem Mol Biol 1:1–30
    [Google Scholar]
  60. Robinson K. M., Lemire B. D. 1996; Covalent attachment of FAD to the yeast succinate dehydrogenase flavoprotein requires import into mitochondria, presequence removal, and folding. J Biol Chem 271:4055–4060
    [Google Scholar]
  61. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
    [Google Scholar]
  62. 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]
  63. Schedel M., Trüper H. G. 1979; Purification of Thiobacillus denitrificans siroheme sulfite reductase and investigation of some molecular and catalytic properties. Biochim Biophys Acta 568:454–467
    [Google Scholar]
  64. Schedel M., Vanselow M., Trüper H. G. 1979; Siroheme sulfite reductase isolated from Chromatium vinosum. Purification and investigation of some of its molecular and catalytic properties. Arch Microbiol 121:29–36
    [Google Scholar]
  65. Schidlowski M. 1986; Evolution of the early sulphur cycle. In Proceedings of the International Meeting on Geochemistry of the Earth Surface and Processes of Mineral Formation, Granada, Spain pp. 29–49 Edited by Rodriguez-Clemente R., Tardy Y. Madrid: Consejo Superior de Investigaciones Cientificas;
    [Google Scholar]
  66. Schrӧder I., Gunsalus R. P., Ackrell B. A. C., Cochran B., Cecchini G. 1991; Identification of active site residues of Escherichia coli fumarate reductase by site-directed mutagenesis. J Biol Chem 266:13572–13579
    [Google Scholar]
  67. Schuler G. D., Altschul S. F., Lipman D. J. 1991; A workbench for multiple alignment construction and analysis. Proteins Struct Fund Genet 9:180–190
    [Google Scholar]
  68. Schwenn J. D., Biere M. 1979; APS-reductase activity in the chromatophores of Chromatium vinosum strain D. FEMS Microbiol Lett 6:19–22
    [Google Scholar]
  69. Skyring G. W., Donnelly T. H. 1982; Precambrian sulfur isotopes and a possible role for sulfite in the evolution of biological sulfate reduction. Precambrian Res 17:41–61
    [Google Scholar]
  70. Speich N., Trüper H. G. 1988; Adenylylsulphate reductase in a dissimilatory sulphate-reducing archaebacterium. J Gen Microbiol 134:1419–1425
    [Google Scholar]
  71. Speich N., Dahl C., Heisig P., Klein A., Lottspeich F., Stetter K. O., Trüper H. G. 1994; Adenylylsulphate reductase from the sulphate-reducing archaeon Archaeoglobus fulgidus: cloning and characterization of the genes and comparison of the enzyme with other iron-sulphur flavoproteins. Microbiology 140:1273–1284
    [Google Scholar]
  72. Takakuwa S. 1992; Biochemical aspects of microbial oxidation of inorganic sulphur compounds. In Organic Sulfur Chemistry: Biochemical Aspects pp. 1–43 Edited by Oae S., Okuyama T. Boca Raton, FL: CRC Press;
    [Google Scholar]
  73. Takezaki N., Rzhetsky A., Nei M. 1995; Phylogenetic test of the molecular clock and linearized trees. Mol Biol Evol 12:823–833
    [Google Scholar]
  74. Thauer R. K. 1989; Energy metabolism of sulfate-reducing bacteria. In Autotrophic Bacteria pp. 397–413 Edited by Schlegel H. G., Bowien B. Madison, WI: Science Tech Publishers;
    [Google Scholar]
  75. Trüper H. G. 1994; Taxonomic notes: names for the higher taxa and their impact on the code of nomenclature of bacteria. Int J Syst Bacteriol 44:368–369
    [Google Scholar]
  76. Trüper H. G., Fischer U. 1982; Anaerobic oxidation of sulfur compounds as electron donors for bacterial photosynthesis. Philos Trans R Soc Lond B Biol Sci 298:529–542
    [Google Scholar]
  77. Verhagen M. F. J., M., Kooter I. M., Wolbert R. B. G., Hagen W. R. 1994; On the iron-sulfur cluster of adenosine phosphosulfate reductase from Desulfovibrio vulgaris (Hildenborough). Eur J Biochem 221:831–837
    [Google Scholar]
  78. Wӓchtershӓuser G. 1988; Pyrite formation, the first energy source for life: a hypothesis. Syst Appl Microbiol 10:207–210
    [Google Scholar]
  79. West M. W., Hecht M. H. 1995; Binary patterning of polar and nonpolar amino acids in the sequences and structures of native proteins. Protein Sci 4:2032–2039
    [Google Scholar]
  80. Wierenga R. K., Terpstra P., HoI W. G. J. 1986; Prediction of the occurrence of the ADP-binding beta-alpha-beta-fold in proteins, using an amino acid sequence fingerprint. J Mol Biol 187:101–107
    [Google Scholar]
  81. Woese C. R. 1987; Bacterial evolution. Microbiol Rev 51:221–271
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-143-9-2891
Loading
/content/journal/micro/10.1099/00221287-143-9-2891
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error