Bifurcated degradative pathway of 3-sulfolactate in Roseovarius nubinhibens ISM via sulfoacetaldehyde acetyltransferase and (S)-cysteate sulfolyase

Journal of Bacteriology

Volumn 191, Issue 18, 2009, Pages 5648-5656

  Denger, Karin ^a   Mayer, Jutta ^a   Buhmann, Matthias ^a   Weinitschke, Sonja ^a   Smits, Theo H M ^a,b   Cook, Alasdair M ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b AGROSCOPE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; BACTERIAL ENZYME; CARBOXYLYASE; CYSTEATE SULFOLYASE; PHOSPHATE ACETYLTRANSFERASE; SULFITE DEHYDROGENASE; SULFOACETALDEHYDE ACETYLTRANSFERASE; SULFOLACTATE SULFOLYASE; SULFOPYRUVATE DECARBOXYLASE; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOCHEMISTRY; BIODEGRADATION; BIOINFORMATICS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME DEGRADATION; ENZYME ISOLATION; ENZYME PURIFICATION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; MARINE BACTERIUM; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROSEOVARIUS NUBINHIBENS; SIGNAL TRANSDUCTION;

ACETALDEHYDE; ACETYLTRANSFERASES; BACTERIAL PROTEINS; CULTURE MEDIA; CYSTEIC ACID; GENE EXPRESSION REGULATION, BACTERIAL; LACTATES; LYASES; RHODOBACTERACEAE; SULFATES;

BACTERIA (MICROORGANISMS); ROSEOVARIUS NUBINHIBENS ISM;

EID: 69949096806     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00569-09     Document Type: Article

References (58)

1. Alber, B. E., R. Spanheimer, C. Ebenau-Jehle, and G. Fuchs. 2006. Study of an alternative glyoxylate cycle for acetate assimilation by Rhodobacter sphaeroides. Mol. Microbiol. 61:297-309.
2. Baldock, M. I., K. Denger, T. H. M. Smits, and A. M. Cook. 2007. Roseovarius sp. strain 217: aerobic taurine dissimilation via acetate kinase and acetate-CoA ligase. FEMS Microbiol. Lett. 271:202-206.
3. Benson, A. A., and R. F. Lee. 1972. The sulphoglycolytic pathway in plants. Biochem. J. 128:29P-30P.
4. Bergmeyer, H. U. 1983. Determination of metabolite concentrations with end-point methods, p. 163-181. In H. U. Bergmeyer (ed.), Methods of enzymic analysis, 3rd ed., vol.1. Verlag Chemie, Weinheim, Germany.
5. Bonsen, P. P. M., J. A. Spudich, D. L. Nelson, and A. Kornberg. 1969. Biochemical studies of bacterial sporulation and germination XII. A sulfonic acid as a major sulfur compound of Bacillus subtilis spores. J. Bacteriol. 98:62-68.
6. Bradford, 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.
7. Cook, A. M. 1987. Biodegradation of s-triazine xenobiotics. FEMS Microbiol. Rev. 46:93-116.
8. 2 sulfonates. Arch. Microbiol. 179:1-6.
9. 3-sulfonates. Arch. Microbiol. 185:83-90.
10. Cook, A. M., T. H. M. Smits, and K. Denger. 2007. Sulfonates and organotrophic sulfite metabolism, p. 170-181. In C. Dahl and C. G. Friedrich (ed.), Microbial sulfur metabolism. Springer Verlag, Berlin, Germany.
11. Cunningham, C., K. F. Tipton, and H. B. F. Dixon. 1998. Conversion of taurine into N-chlorotaurine (taurine chloramine) and sulphoacetaldehyde in response to oxidative stress. Biochem. J. 330:939-945.
12. Denger, K., and A. M. Cook. 2001. Ethanedisulfonate is degraded via sulfoacetaldehyde in Ralstonia sp. strain EDS1. Arch. Microbiol. 176:89-95.
13. Denger, K., J. Ruff, U. Rein, and A. M. Cook. 2001. Sulfoacetaldehyde sulfo-lyase (EC 4.4.1.12) from Desulfonispora thiosulfatigenes: purification, properties and primary sequence. Biochem. J. 357:581-586.
14. Denger, K., T. H. M. Smits, and A. M. Cook. 2006. L-Cysteate sulfo-lyase, a widespread, pyridoxal 5-phosphate-coupled desulfonative enzyme purified from Silicibacter pomeroyi DSS-3T. Biochem. J. 394:657-664.
15. Denger, K., S. Weinitschke, K. Hollemeyer, and A. M. Cook. 2004. Sulfoacetate generated by Rhodopseudomonas palustris from taurine. Arch. Microbiol. 182:254-258.
16. Denger, K., S. Weinitschke, T. H. M. Smits, D. Schleheck, and A. M. Cook. 2008. Bacterial sulfite dehydrogenases in organotrophic metabolism: separation and identification in Cupriavidus necator H16 and in Delftia acidovorans SPH-1. Microbiology (Reading, England) 154:256-263. (Pubitemid 351201405)
17. Eichhorn, E., J. R. van der Ploeg, M. A. Kertesz, and T. Leisinger. 1997. Characterization of α-ketoglutarate-dependent taurine dioxygenase from Escherichia coli. J. Biol. Chem. 272:23031-23036.
18. Giovannoni, S., and M. Rappé. 2000. Evolution, diversity, and molecular ecology of marine prokaryotes, p. 47-84. In D. L. Kirchman (ed.), Microbial ecology of the oceans. Wiley-Liss, New York, NY.
19. González, J. M., J. S. Covert, W. B. Whitman, J. R. Henriksen, F. Mayer, B. Scharf, R. Schmitt, A. Buchan, J. A. Fuhrman, R. P. Kiene, and M. A. Moran. 2003. Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int. J. Syst. Evol. Microbiol. 53:1261-1269.
20. González, J. M., R. Simó, R. Massana, J. S. Covert, E. O. Casamayor, C. Pedrós-Alió, and M. A. Moran. 2000. Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl. Environ. Microbiol. 66:4237-4246.
21. Gorzynska, A. K., K. Denger, A. M. Cook, and T. H. M. Smits. 2006. Inducible transcription of genes involved in taurine uptake and dissimilation by Silicibacter pomeroyi DSS-3T. Arch. Microbiol. 185:402-406.
22. Graham, D. E., and R. H. White. 2002. Elucidation of methanogenic coenzyme biosyntheses: from spectroscopy to genomics. Nat. Prod. Rep. 19:133-147.
23. Graham, D. E., H. Xu, and R. H. White. 2002. Identification of coenzyme M biosynthetic phosphosulfolactate synthase: a new family of sulfonate biosynthesizing enzymes. J. Biol. Chem. 277:13421-13429.
24. Graupner, M., H. Xu, and R. H. White. 2000. Identification of an archaeal 2-hydroxy acid dehydrogenase catalyzing reactions involved in coenzyme biosynthesis in methanoarchaea. J. Bacteriol. 182:3688-3692. (Pubitemid 30413019)
25. Graupner, M., H. Xu, and R. H. White. 2000. Identification of the gene encoding sulfopyruvate decarboxylase, an enzyme involved in biosynthesis of coenzyme M. J. Bacteriol. 182:4862-4867. (Pubitemid 30641810)
26. Junker, F., T. Leisinger, and A. M. Cook. 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 (Reading, England) 140:1713-1722. (Pubitemid 24231160)
27. Kahnert, A., and M. A. Kertesz. 2000. Characterization of a sulfur-regulated oxygenative alkylsulfatase from Pseudomonas putida S-313. J. Biol. Chem. 275:31661-31667.
28. Kappler, U., B. Bennett, J. Rethmeier, G. Schwarz, R. Deutzmann, A. G. McEwan, and C. Dahl. 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.
29. Kearney, E. B., and P. P. Singer. 1953. Enzymic transformations of L-cysteinesulfinic acid. Biochim. Biophys. Acta 11:276-289.
30. Kelly, D. P., and J. C. Murrell. 1999. Microbial metabolism of methanesulfonic acid. Arch. Microbiol. 172:341-348.
31. Kennedy, S. I. T., and C. A. Fewson. 1968. Enzymes of the mandelate pathway in bacterium N.C.I.B. 8250. Biochem. J. 107:497-506.
32. Kertesz, M. A. 2004. Metabolism of sulphur-containing organic compounds, p. 323-357. In J. Ramos (ed.), Pseudomonas, vol.3. Wiley, New York, NY.
33. Krejčík, Z., K. Denger, S. Weinitschke, K. Hollemeyer, V. Pačes, A. M. Cook, and T. H. M. Smits. 2008. Sulfoacetate released during the assimilation of taurine-nitrogen by Neptuniibacter caesariensis: purification of sulfoacetaldehyde dehydrogenase. Arch. Microbiol. 190:159-168.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Laue, H., K. Denger, and A. M. Cook. 1997. Taurine reduction in anaerobic respiration of Bilophila wadsworthia RZATAU. Appl. Environ. Microbiol. 63:2016-2021.
36. Martelli, H. L., and A. A. Benson. 1964. Sulfocarbohydrate metabolism 1. Bacterial production and utilization of sulfoacetate. Biochim. Biophys. Acta 93:169-171.
37. Mayer, J., K. Denger, T. H. M. Smits, K. Hollemeyer, U. Groth, and A. M. Cook. 2006. N-Acetyltaurine dissimilated via taurine by Delftia acidovorans NAT. Arch. Microbiol. 186:61-67.
38. Mikosch, C., K. Denger, E.-M. Schäfer, and A. M. Cook. 1999. Anaerobic oxidations of cysteate: degradation via a cysteate:2-oxoglutarate aminotransferase in Paracoccus pantotrophus. Microbiology (Reading, England) 145:1153-1160.
39. Quick, A., N. J. Russell, S. G. Hales, and G. F. White. 1994. Biodegradation of sulphosuccinate: direct desulphonation of a secondary sulphonate. Microbiology (Reading, England) 140:2991-2998. (Pubitemid 24359527)
40. Racker, E. 1962. Fructose-6-phosphate phosphoketolase from Acetobacter xylinum. Methods Enzymol. 5:276-280.
41. Reichenbecher, W., D. P. Kelly, and J. C. Murrell. 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.
42. Rein, U., R. Gueta, K. Denger, J. Ruff, K. Hollemeyer, and A. M. Cook. 2005. Dissimilation of cysteate via 3-sulfolactate sulfo-lyase and a sulfate exporter in Paracoccus pantotrophus NKNCYSA. Microbiology (Reading, England) 151:737-747.
43. Rösch, V., K. Denger, D. Schleheck, T. H. M. Smits, and A. M. Cook. 2008. Different bacterial strategies to degrade taurocholate. Arch. Microbiol. 190:11-18.
44. Roy, A. B., M. J. E. Hewlins, A. J. Ellis, J. L. Harwood, and G. F. White. 2003. Glycolytic breakdown of sulfoquinovose in bacteria: a missing link in the sulfur cycle. Appl. Environ. Microbiol. 69:6434-6441.
45. Ruff, J., K. Denger, and A. M. Cook. 2003. Sulphoacetaldehyde acetyltransferase yields acetyl phosphate: purification from Alcaligenes defragrans and gene clusters in taurine degradation. Biochem. J. 369:275-285.
46. Schäfer, H., I. R. McDonald, P. D. Nightingale, and J. C. Murrell. 2005. Evidence for the presence of a CmuA methyltransferase pathway in novel marine methyl halide-oxidizing bacteria. Environ. Microbiol. 7:839-852.
47. Schmidt, E. 1974. Glutamat-dehydrogenase UV-test, p. 689-696. In H. U. Bergmeyer (ed.), Methoden der enzymatischen analyse. Verlag Chemie, Weinheim, Germany.
48. Shibuya, I., T. Yagi, and A. A. Benson. 1963. Sulfonic acids in algae, p. 627-636. In Japanese Society of Plant Physiologists (ed.), Studies on microalgae and photosynthetic bacteria. University of Tokyo Press, Tokyo, Japan.
49. Sörbo, B. 1987. Sulfate: turbidimetric and nephelometric methods. Methods Enzymol. 143:3-6.
50. Styp von Rekowski, K., K. Denger, and A. M. Cook. 2005. Isethionate as a product from taurine during nitrogen-limited growth of Klebsiella oxytoca Tau-N1. Arch. Microbiol. 183:325-330.
51. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
52. Weinitschke, S., K. Denger, T. H. M. Smits, K. Hollemeyer, and A. M. Cook. 2006. The sulfonated osmolyte N-methyltaurine is dissimilated by Alcaligenes faecalis and by Paracoccus versutus with release of methylamine. Microbiology (Reading, England) 152:1179-1186.
53. Weinitschke, S., K. Styp von Rekowski, K. Denger, and A. M. Cook. 2005. Sulfoacetaldehyde is excreted quantitatively by Acinetobacter calcoaceticus SW1 during growth with taurine as sole source of nitrogen. Microbiology (Reading, England) 151:1285-1290.
54. Weinstein, C. L., and O. W. Griffith. 1988. Cysteinesulfonate and β-sulfopyruvate metabolism. Partitioning between decarboxylation, transamination, and reduction pathways. J. Biol. Chem. 263:3735-3743.
55. White, R. H. 1986. Intermediates in the biosynthesis of coenzyme M (2-mercaptoethanesulfonic acid). Biochemistry 25:5304-5308.
56. Winnen, B., R. N. Hvorup, and M. H. Saier, Jr. 2003. The tripartite tricarboxylate transporter (TTT) family. Res. Microbiol. 154:457-465.
57. Yagi, T., H. Kagamiyama, and M. Nozaki. 1979. Cysteine sulfinate transamination activity of aspartate aminotransferases. Biochem. Biophys. Res. Commun. 90:447-452.
58. Yi, H., Y. W. Lim, and J. Chun. 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. (Pubitemid 46711965)