Bacterial sulfite dehydrogenases in organotrophic metabolism: separation and identification in H16 and in SPH-1 Free

Abstract

The utilization of organosulfonates as carbon sources by aerobic or nitrate-reducing bacteria usually involves a measurable, uncharacterized sulfite dehydrogenase. This is tacitly assumed to be sulfite : ferricytochrome- oxidoreductase [EC 1.8.2.1], despite negligible interaction with (eukaryotic) cytochrome : the enzyme is assayed at high specific activity with ferricyanide as electron acceptor. Purified periplasmic sulfite dehydrogenases (SorAB, SoxCD) are known from chemoautotrophic growth and are termed ‘sulfite oxidases’ by bioinformatic services. The catalytic unit (SorA, SoxC; termed ‘sulfite oxidases’ cd02114 and cd02113, respectively) binds a molybdenum-cofactor (Moco), and involves a cytochrome (SorB, SoxD) as electron acceptor. The genomes of several bacteria that express a sulfite dehydrogenase during heterotrophic growth contain neither nor genes; others contain at least four paralogues, for example H16, which is known to express an inducible sulfite dehydrogenase during growth with taurine (2-aminoethanesulfonate). This soluble enzyme was enriched 320-fold in four steps. The 40 kDa protein (denatured) had an -terminal amino acid sequence which started at position 42 of the deduced sequence of H16_B0860 (termed ‘sulfite oxidase’ cd02114), which we named SorA. The neighbouring gene is an orthologue of , and the genes were co-transcribed. Cell fractionation showed SorA to be periplasmic. The corresponding enzyme in SPH-1 was enriched 270-fold, identified as Daci_0055 (termed ‘sulfite oxidase’ cd02110) and has a cytochrome encoded downstream. We presume, from genomic data for bacteria and archaea, that there are several subgroups of sulfite dehydrogenases, which all contain a Moco, and transfer electrons to a specific cytochrome .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/011650-0
2008-01-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/1/256.html?itemId=/content/journal/micro/10.1099/mic.0.2007/011650-0&mimeType=html&fmt=ahah

References

  1. Beller H. R., Chain P. S. G., Letain T. E., Chakicherla A., Larimer F. W., Richardson P. M., Coleman M. A., Wood A. P., Kelly D. P. 2006; The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans . J Bacteriol 188:1473–1488
    [Google Scholar]
  2. Bendtsen J. D., Nielsen H., von Heijne G., Brunak S. 2004; Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795
    [Google Scholar]
  3. 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
    [Google Scholar]
  4. Chan L.-K., Morgan-Kiss R., Hanson T. E. 2007; Sulfur oxidation in Chlorobium tepidum (syn. Chlorobaculum tepidum ): genetic and proteomic analyses. In Microbial Sulfur Metabolism pp 117–126 Edited by Dahl C., Friedrich C. G. Berlin: Springer Verlag;
    [Google Scholar]
  5. Cook A. M., Smits T. H. M., Denger K. 2007; Sulfonates and organotrophic sulfite metabolism. In Microbial Sulfur Metabolism pp 170–183 Edited by Dahl C., Friedrich C. G. Berlin: Springer Verlag;
    [Google Scholar]
  6. Denger K., Ruff J., Rein U., Cook A. M. 2001; Sulfoacetaldehyde sulfo-lyase [EC 4.4.1.12] from Desulfonispora thiosulfatigenes : purification, properties and primary sequence. Biochem J 357:581–586
    [Google Scholar]
  7. Desomer J., Crespi M., Van Montagu M. 1991; Illegitimate integration of non-replicative vectors in the genome of Rhodococcus fascians upon electro-transformation as an insertional mutagenesis system. Mol Microbiol 5:2115–2124
    [Google Scholar]
  8. Doonan C. J., Kappler U., George G. N. 2006; Structure of the active site of sulfite dehydrogenase from Starkeya novella . Inorg Chem 45:7488–7492
    [Google Scholar]
  9. Francis R. T. Jr, Becker R. R. 1984; Specific indication of hemoproteins in polyacrylamide gels using a double-staining process. Anal Biochem 136:509–514
    [Google Scholar]
  10. Friedrich C. G., Quentmeier A., Bardischewsky F., Rother D., Orawski G., Hellwig P., Fischer J. 2007; Redox control of chemotrophic sulfur oxidation of Paracoccus pantotrophus . In Microbial Sulfur Metabolism pp 139–150 Edited by Dahl C. Friedrich C. G. Berlin: Springer Verlag;
    [Google Scholar]
  11. Fritz G., Schiffer A., Behrens A., Büchert T., Ermler U., Kroneck P. M. H. 2007; Living on sulfate: three-dimensional structure and spectroscopy of adenosine 5′-phosphosulfate reductase and dissimilatory sulfite reductase. In Microbial Sulfur Metabolism pp 13–23 Edited by Dahl C. Friedrich C. G. Berlin: Springer Verlag;
    [Google Scholar]
  12. Gorzynska A. K., Denger K., Cook A. M., Smits T. H. M. 2006; Inducible transcription of genes involved in taurine uptake and dissimilation by Silicibacter pomeroyi DSS-3T . Arch Microbiol 185:402–406
    [Google Scholar]
  13. Innis M. A., Gelfand D. H., Sninsky J. J., White T. J. 1990 PCR Protocols. A Guide to Methods and Applications San Diego: Academic Press, Inc;
  14. Johnston J. B., Murray K., Cain R. B. 1975; Microbial metabolism of aryl sulphonates. A reassessment of colorimetric methods for the determination of sulphite and their use in measuring desulphonation of aryl and alkylbenzene sulphonates. Antonie Van Leeuwenhoek 41:493–511
    [Google Scholar]
  15. Junker F., Leisinger T., Cook A. M. 1994; 3-Sulphocatechol 2,3-dioxygenase and other dioxygenases (EC 1.13.11.2 and EC 1.14.12.–) in the degradative pathways of 2-aminobenzenesulphonic, benzenesulphonic and 4-toluenesulphonic acids in Alcaligenes sp. strain O-1. Microbiology 140:1713–1722
    [Google Scholar]
  16. Kappler U. 2007; Bacterial sulfite-oxidizing enzymes – enzymes for chemolithotrophs only?. In Microbial Sulfur Metabolism pp 151–169 Edited by Dahl C. Friedrich C. G. Berlin: Springer Verlag;
    [Google Scholar]
  17. Kappler U., Bennett B., Rethmeier J., Schwarz G., Deutzmann R., McEwan A. G., Dahl C. 2000; Sulfite : cytochrome c oxidoreductase from Thiobacillus novellus . Purification, characterization, and molecular biology of a heterodimeric member of the sulfite oxidase family. J Biol Chem 275:13202–13212
    [Google Scholar]
  18. Kelly D. P., Shergill J. K., Lu W. P., Wood A. P. 1997; Oxidative metabolism of inorganic sulfur compounds by bacteria. Antonie Van Leeuwenhoek 71:95–107
    [Google Scholar]
  19. King J. E., Quinn J. P. 1997; Metabolism of sulfoacetate by environmental Aureobacterium sp. and Comamonas acidovorans isolates. Microbiology 143:3907–3912
    [Google Scholar]
  20. King J. E., Jaouhari R., Quinn J. P. 1997; The role of sulfoacetaldehyde sulfo-lyase in the mineralization of isethionate by an environmental Acinetobacter isolate. Microbiology 143:2339–2343
    [Google Scholar]
  21. Kondo H., Ishimoto M. 1972; Enzymatic formation of sulfite and acetate from sulfoacetaldehyde, a degradation product of taurine. J Biochem ( Tokyo ) 72:487–489
    [Google Scholar]
  22. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
    [Google Scholar]
  23. Laue H., Field J. A., Cook A. M. 1996; Bacterial desulfonation of the ethanesulfonate metabolite of the chloroacetanilide herbicide metazachlor. Environ Sci Technol 30:1129–1132
    [Google Scholar]
  24. le Maire M., Ghasi A., Moller J. V. 1996; Gel chromatography as an analytical tool for characterization of size and molecular mass of proteins. ACS Symp Ser 635:36–51
    [Google Scholar]
  25. Lu W.-P., Kelly D. P. 1984; Properties and role of sulphite: cytochrome c oxidoreductase purified from Thiobacillus versutus (A2). J Gen Microbiol 130:1683–1692
    [Google Scholar]
  26. Marchler-Bauer A., Anderson J. B., Derbyshire M. K., DeWeese-Scott C., Gonzalez N. R., Gwadz M., Hao L., He S., Hurwitz D. I. other authors 2007; CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 35:D237–D240
    [Google Scholar]
  27. Mayer J., Denger K., Smits T. H. M., Hollemeyer K., Groth U., Cook A. M. 2006; N -Acetyltaurine dissimilated via taurine by Delftia acidovorans NAT. Arch Microbiol 186:61–67
    [Google Scholar]
  28. Metzler D. E. 2001 Biochemistry: the Chemical Reactions of Living Cells , 2nd edn. San Diego: Academic Press;
  29. Pohlmann A., Fricke W. F., Reinecke F., Kusian B., Liesegang H., Cramm R., Eitinger T., Ewering C., Pötter M. other authors 2006; Genome sequence of the bioplastic-producing “Knallgas” bacterium Ralstonia eutropha H16. Nat Biotechnol 24:1257–1262
    [Google Scholar]
  30. Reichenbecher W., Kelly D. P., Murrell J. C. 1999; Desulfonation of propanesulfonic acid by Comamonas acidovorans strain P53: evidence for an alkanesulfonate sulfonatase and an atypical sulfite dehydrogenase. Arch Microbiol 172:387–392
    [Google Scholar]
  31. Ruff J., Denger K., Cook A. M. 2003; Sulphoacetaldehyde acetyltransferase yields acetyl phosphate: purification from Alcaligenes defragrans and gene clusters in taurine degradation. Biochem J 369:275–285
    [Google Scholar]
  32. Schiffer A., Fritz G., Kroneck P. M. H., Ermler U. 2006; Reaction mechanism of the iron-sulfur flavoenzyme adenosine-5′-phosphosulfate reductase based on the structural characterization of different enzymatic states. Biochemistry 45:2960–2967
    [Google Scholar]
  33. Schleheck D., Knepper T. P., Fischer K., Cook A. M. 2004; Mineralization of individual congeners of linear alkylbenzenesulfonate (LAS) by defined pairs of heterotrophic bacteria. Appl Environ Microbiol 70:4053–4063
    [Google Scholar]
  34. Sörbo B. 1987; Sulfate: turbidimetric and nephelometric methods. Methods Enzymol 143:3–6
    [Google Scholar]
  35. Thurnheer T., Köhler T., Cook A. M., Leisinger T. 1986; Orthanilic acid and analogues as carbon sources for bacteria: growth physiology and enzymic desulfonation. J Gen Microbiol 132:1215–1220
    [Google Scholar]
  36. Thysse G. J. E., Wanders T. H. 1974; Initial steps in the degradation of n -alkane-1-sulphonates by Pseudomonas . Antonie Van Leeuwenhoek 40:25–37
    [Google Scholar]
  37. Toghrol F., Southerland W. M. 1983; Purification of Thiobacillus novellus sulfite oxidase. Evidence for the presence of heme and molybdenum. J Biol Chem 258:6762–6766
    [Google Scholar]
  38. Weinitschke S., Styp von Rekowski K., Denger K., Cook A. M. 2005; Sulfoacetaldehyde is excreted quantitatively by Acinetobacter calcoaceticus SW1 during growth with taurine as sole source of nitrogen. Microbiology 151:1285–1290
    [Google Scholar]
  39. Weinitschke S., Denger K., Cook A. M., Smits T. H. M. 2007; The DUF81 protein TauE in Cupriavidus necator H16, a sulfite exporter in the metabolism of C2 sulfonates. Microbiology 153:3055–3060
    [Google Scholar]
  40. Weisburg W. G., Barns S. M., Pelletier D. A., Lane D. J. 1991; 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
    [Google Scholar]
  41. Witholt B., Boekhout M., Brock M., Kingma J., Heerikhuizen H. V., Leij L. D. 1976; An efficient and reproducible procedure for the formation of spheroplasts from variously grown Escherichia coli . Anal Biochem 74:160–170
    [Google Scholar]
  42. Wodara C., Bardischewsky F., Friedrich C. G. 1997; 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. J Bacteriol 179:5014–5023
    [Google Scholar]
  43. Yi H., Lim Y. W., Chun J. 2007; Taxonomic evaluation of the genera Ruegeria and Silicibacter : a proposal to transfer the genus Silicibacter Petursdottir and Kristjansson 1999 to the genus Ruegeria Uchino et al. 1999. Int J Syst Evol Microbiol 57:815–819
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/011650-0
Loading
/content/journal/micro/10.1099/mic.0.2007/011650-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed