1887

Microbiology Society logo

Volume 150, Issue 4

Enzymes and genes of taurine and isethionate dissimilation in Free

Abstract

Growth of the -proteobacterium NKNIS with taurine or isethionate as sole source of carbon involves sulfoacetaldehyde acetyltransferase (Xsc), which is presumably encoded by an gene in subgroup 3, none of whose gene products has been characterized. The genome of the -proteobacterium 2.4.1 was interpreted to contain a nine-gene cluster encoding the inducible dissimilation of taurine, and this deduced pathway included a regulator, a tripartite ATP-independent transporter, taurine dehydrogenase (TDH; presumably TauXY) as well as Xsc (subgroup 3), a hypothetical protein and phosphate acetyltransferase (Pta). A similar cluster was found in NKNIS, in contrast to an analogous cluster encoding an ATP-binding cassette transporter in . Inducible TDH, Xsc and Pta were found in extracts of taurine-grown cells of strain NKNIS. TDH oxidized taurine to sulfoacetaldehyde and ammonium ion with cytochrome as electron acceptor. Whereas Xsc and Pta were soluble enzymes, TDH was located in the particulate fraction, where inducible proteins with the expected masses of TauXY (14 and 50 kDa, respectively) were detected by SDS-PAGE. Xsc and Pta were separated by anion-exchange chromatography. Xsc was effectively pure; the molecular mass of the subunit (64 kDa) and the N-terminal amino acid sequence confirmed the identification of the gene. Inducible isethionate dehydrogenase (IDH), Xsc and Pta were assayed in extracts of isethionate-grown cells of strain NKNIS. IDH was located in the particulate fraction, oxidized isethionate to sulfoacetaldehyde with cytochrome as electron acceptor and correlated with the expression of a 62 kDa protein. Strain NKNIS excreted sulfite and sulfate during growth with a sulfonate and no sulfite dehydrogenase was detected. There is considerable biochemical, genetic and regulatory complexity in the degradation of these simple molecules.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): ABC transporter, ATP-binding cassette transporter , DCPIP, dichlorophenol indophenol , IDH, isethionate dehydrogenase , MALDI-TOF-MS, matrix-assisted, laser-desorption ionization time-of-flight mass spectrometry , Pta, phosphate acetyltransferase , TDH, taurine dehydrogenase , ThDP, thiamin diphosphate , Tpa, taurine : pyruvate aminotransferase , TRAP transporter, tripartite ATP-independent transporter and Xsc, sulfoacetaldehyde acetyltransferase
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26795-0
2004-04-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/4/mic1500805.html?itemId=/content/journal/micro/10.1099/mic.0.26795-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden T. L., Zhang Z., Miller W., Lipman D. J., Schäffer A. A., Zhang J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
     [Google Scholar]
  2. Bar-Ilan A., Balan V., Tittmann K., Golbik R., Vyazmensky M., Hubner G., Barak Z., Chipman D. M. 2001; Binding and activation of thiamin diphosphate in acetohydroxyacid synthase. Biochemistry 40:11946–11954 [CrossRef]
     [Google Scholar]
  3. Ben-Bassat A., Bauer K., Chang S. Y., Myambo K., Boosman A., Chang S. 1987; Processing of the initiation methionine from proteins: properties of the Escherichia coli methionine aminopeptidase and its gene structure. J Bacteriol 169:751–757
     [Google Scholar]
  4. Bergmeyer H. U. 1983; Determination of metabolite concentrations with end-point methods. In Methods of Enzymic Analysis vol 1 pp. 163–181 Edited by Bergmeyer H. U. Weinheim: Verlag Chemie;
     [Google Scholar]
  5. Bergmeyer H. U., Graßl M., Walter E.-M. 1983; Phosphotransacetylase. In Methods of Enzymatic Analysis vol 2 pp. 295–296 Edited by Bergmeyer H. U. Weinheim: Verlag Chemie;
     [Google Scholar]
  6. Chance B., Williams G. R. 1955; Respiratory enzymes in oxidative phosphorylation. II. Difference spectra. J Biol Chem 217:395–407
     [Google Scholar]
  7. Cook A. M., Denger K. 2002; Dissimilation of the C2 sulfonates. Arch Microbiol 179:1–6 [CrossRef]
     [Google Scholar]
  8. Cunningham C., Tipton K. F., Dixon H. B. F. 1998; Conversion of taurine into N-chlorotaurine (taurine chloramine) and sulphoacetaldehyde in response to oxidative stress. Biochem J 330:939–945
     [Google Scholar]
  9. de Marco P., Moradas-Ferreira P., Higgins T. P., McDonald I., Kenna E. M., Murrell J. C. 1999; Molecular analysis of a novel methanesulfonic acid monooxygenase from the methylotroph Methylosulfonomonas methylovora. J Bacteriol 181:2244–2251
     [Google Scholar]
  10. Denger K., Cook A. M. 2001; Ethanedisulfonate is degraded via sulfoacetaldehyde in Ralstonia sp. strain EDS1. Arch Microbiol 176:89–95 [CrossRef]
     [Google Scholar]
  11. Denger K., Laue H., Cook A. M. 1997; Anaerobic taurine oxidation: a novel reaction by a nitrate-reducing Alcaligenes sp. Microbiology 143:1919–1924 [CrossRef]
     [Google Scholar]
  12. 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 structure. Biochem J 357:581–586 [CrossRef]
     [Google Scholar]
  13. Ehrmann M., Ehrle R., Hofmann E., Boos W., Schlosser A. 1998; The ABC maltose transporter. Mol Microbiol 29:685–694 [CrossRef]
     [Google Scholar]
  14. Ensley B. D., Gibson D. T., Laborde A. L. 1982; Oxidation of naphthalene by a multicomponent enzyme system from Pseudomonas sp. strain NCIB 9816 J Bacteriol 149:948–954
     [Google Scholar]
  15. Fellman J. H., Roth E. S., Avedovech N. A., McCarthy K. D. 1980; The metabolism of taurine to isethionate. Arch Biochem Biophys 204:560–567 [CrossRef]
     [Google Scholar]
  16. Finan T. M., Weidner S., Wong K.9 other authors 2001; The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiontSinorhizobium meliloti. Proc Natl Acad Sci U S A 98:9889–9894 [CrossRef]
     [Google Scholar]
  17. Gesellschalt Deutscher Chemiker. 1996 German Standard Methods for the Laboratory Examination of Water, Waste Water and Sludge Weinheim: VCH;
  18. Huxtable R. J. 1992; Physiological actions of taurine. Physiol Rev 72:101–163
     [Google Scholar]
  19. Jones K. M. 1979; Artificial substrates and biochemical reagents. In Data for Biochemical Research pp. 436–465 Edited by Dawson R. M. C. , Elliott D. C., Elliott W. H., Jones K. M. Oxford. Oxford University Press;
     [Google Scholar]
  20. Jovanovic G., Model P. 1997; The RIB element in the goaG-pspF intergenic region of Escherichia coli. J Bacteriol 179:3095–3102
     [Google Scholar]
  21. 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 [CrossRef]
     [Google Scholar]
  22. Kappler U., Dahl C. 2001; Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol Lett 203:1–9 [CrossRef]
     [Google Scholar]
  23. Kelly D. J., Thomas G. H. 2001; The tripartite ATP-independent periplasmic (TRAP) transporters of bacteria and archaea. FEMS Microbiol Rev 25:405–424 [CrossRef]
     [Google Scholar]
  24. Kertesz M. A. 2000; Riding the sulfur cycle – metabolism of sulfonates and sulfate esters in Gram-negative bacteria. FEMS Microbiol Rev 24:135–175
     [Google Scholar]
  25. Kertesz M. A. 2001; Bacterial transporters for sulfate and organosulfur compounds. Res Microbiol 152:279–290 [CrossRef]
     [Google Scholar]
  26. King J. E., Quinn J. P. 1997; Metabolism of sulfoacetate by environmental Aureobacterium sp. and Comamonas acidovorans isolates. Microbiology 143:3907–3912 [CrossRef]
     [Google Scholar]
  27. 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 [CrossRef]
     [Google Scholar]
  28. Kondo H., Ishimoto M. 1987; Taurine dehydrogenase. Methods Enzymol 143:496–499
     [Google Scholar]
  29. Kondo H., Anada H., Ohsawa K., Ishimoto M. 1971; Formation of sulfoacetaldehyde from taurine in bacterial extracts. J Biochem 69:621–623
     [Google Scholar]
  30. Kondo H., Kagotani K., Oshima M., Ishimoto M. 1973; Purification and some properties of taurine dehydrogenase from a bacterium. J Biochem 73:1269–1278
     [Google Scholar]
  31. Kondo H., Niki H., Takahashi S., Ishimoto M. 1977; Enzymatic oxidation of isethionate to sulfoacetaldehyde in bacterial extract. J Biochem 81:1911–1916
     [Google Scholar]
  32. Kondo H., Yazawa M., Enami M., Ishimoto M. 1982; Sulfite production from benzenesulfonate by bacterial enzyme compared with taurine. Ganryu Aminosan 5:237–242
     [Google Scholar]
  33. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
     [Google Scholar]
  34. Laue H., Cook A. M. 2000; Biochemical and molecular characterization of taurine : pyruvate transaminase from the anaerobe Bilophila wadsworthia. Eur J Biochem 267:6841–6848 [CrossRef]
     [Google Scholar]
  35. Laue H., Denger K., Cook A. M. 1997; Taurine reduction in anaerobic respiration of Bilophila wadsworthia RZATAU. Appl Environ Microbiol 63:2016–2021
     [Google Scholar]
  36. Lee M. H., Scherer M., Rigali S., Golden J. W. 2003; PlmA, a new member of the GntR family, has plasmid maintenance functions in Anabaena sp. strain PCC 7120. J Bacteriol 185:4315–4325 [CrossRef]
     [Google Scholar]
  37. Lie T. L., Leadbetter J. R., Leadbetter E. R. 1998; Metabolism of sulfonic acids and other organosulfur compounds by sulfate-reducing bacteria. Geomicrobiol J 15:135–149 [CrossRef]
     [Google Scholar]
  38. Meier-Wagner J., Nolden L., Jakoby M., Siewe R., Kramer R., Burkovski A. 2001; Multiplicity of ammonium uptake systems in Corynebacterium glutamicum: role of Amt and AmtB. Microbiology 147:135–143
     [Google Scholar]
  39. Mikosch C., Denger K., Schäfer E.-M., Cook A. M. 1999; Anaerobic oxidations of cysteate: degradation via a cysteate : 2-oxoglutarate aminotransferase in Paracoccus pantotrophus. Microbiology 145:1153–1160 [CrossRef]
     [Google Scholar]
  40. Racker E. 1962; Fructose-6-phosphate phosphoketolase from Acetobacter xylinum. Methods Enzymol 5:276–280
     [Google Scholar]
  41. Reese M. G., Harris N. L., Eeckman F. H. 1996; Large scale sequencing specific neural networks for promoter and splice site recognition. In Biocomputing: Proceedings of the 1996 Pacific Symposium pp. 737–738 Edited by Hunter L., Klein T. E. Singapore: World Scientific Publishing;
     [Google Scholar]
  42. 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 [CrossRef]
     [Google Scholar]
  43. Rein U. 1999 Abbauweg(e) für Cysteat bei anaeroben Bakterien Diplomarbeit: University of Konstanz; Konstanz, Germany:
     [Google Scholar]
  44. Rigali S., Derouaux A., Giannotta F., Dusart J. 2002; Subdivision of the helix–turn–helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J Biol Chem 277:12507–12515 [CrossRef]
     [Google Scholar]
  45. 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 [CrossRef]
     [Google Scholar]
  46. Saier M. H., Jr. 1999; A functional-phylogenetic system for the classification of transport proteins. J Cell Biochem Suppl 32:3384–94
     [Google Scholar]
  47. Sanders H. K., Becker G. E., Nason A. 1972; Glycine-cytochrome c reductase from Nitrobacter agilis. J Biol Chem 247:2015–2025
     [Google Scholar]
  48. Sörbo B. 1987; Sulfate: turbidimetric and nephelometric methods. Methods Enzymol 143:3–6
     [Google Scholar]
  49. Stadtman E. R. 1957; Preparation and assay of acetyl phosphate. Methods Enzymol 3:228–231
     [Google Scholar]
  50. Tholey A., Wittmann C., Kang M. J., Bungert D., Hollemeyer K., Heinzle E. 2002; Derivatization of small biomolecules for optimized matrix-assisted laser desorption/ionization mass spectrometry. J Mass Spectrom 37:963–973 [CrossRef]
     [Google Scholar]
  51. Thurnheer T., Leisinger T., Köhler T., Cook A. M. 1986; Orthanilic acid and analogues as carbon sources for bacteria: growth physiology and enzymic desulphonation. J Gen Microbiol 132:1215–1220
     [Google Scholar]
  52. Voet D., Voet J. G., Pratt C. W. 1999 Fundamentals of Biochemistry New York: Wiley;
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26795-0
Loading
Enzymes and genes of taurine and isethionate dissimilation in Paracoccus denitrificans
Microbiology 150, 805 (2004); https://doi.org/10.1099/mic.0.26795-0
/content/journal/micro/10.1099/mic.0.26795-0
/content/journal/micro/10.1099/mic.0.26795-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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