Dissimilation of cysteate via 3-sulfolactate sulfo-lyase and a sulfate exporter in NKNCYSA Free

Abstract

NKNCYSA utilizes ()-cysteate (2-amino-3-sulfopropionate) as a sole source of carbon and energy for growth, with either nitrate or molecular oxygen as terminal electron acceptor, and the specific utilization rate of cysteate is about 2 mkat (kg protein). The initial degradative reaction is catalysed by an ()-cysteate : 2-oxoglutarate aminotransferase, which yields 3-sulfopyruvate. The latter was reduced to 3-sulfolactate by an NAD-linked sulfolactate dehydrogenase [3·3 mkat (kg protein)]. The inducible desulfonation reaction was not detected initially in cell extracts. However, a strongly induced protein with subunits of 8 kDa () and 42 kDa () was found and purified. The corresponding genes had similarities to those encoding altronate dehydratases, which often require iron for activity. The purified enzyme could then be shown to convert 3-sulfolactate to sulfite and pyruvate and it was termed sulfolactate sulfo-lyase (Suy). A high level of sulfite dehydrogenase was also induced during growth with cysteate, and the organism excreted sulfate. A putative regulator, OrfR, was encoded upstream of on the reverse strand. Downstream of was , which was cotranscribed with . The gene, an allele of , encoded a putative membrane protein with transmembrane helices (COG2855), and is a candidate to encode the sulfate exporter needed to maintain homeostasis during desulfonation. -like genes are widespread in sequenced genomes and environmental samples where, in contrast to the current annotation, several presumably encode the desulfonation of 3-sulfolactate, a component of bacterial spores.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27548-0
2005-03-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/3/mic1510737.html?itemId=/content/journal/micro/10.1099/mic.0.27548-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden T. L., Zhang J., Zhang Z., Miller W., Lipman D. J, Schäffer A. A. 1997; Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
    [Google Scholar]
  2. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. 1987 Current Protocols in Molecular Biology New York: Wiley;
    [Google Scholar]
  3. Babbitt P. C., Hasson M. S., Wedekind J. E. & 7 other authors; 1996; The enolase superfamily: a general strategy for enzyme-catalyzed abstraction of the α-protons of carboxylic acids. Biochemistry 35:16489–16501 [CrossRef]
    [Google Scholar]
  4. Bonsen P. P. M., Spudich J. A., Nelson D. L., Kornberg A XII. 1969; Biochemical studies of bacterial sporulation and germination. A sulfonic acid as a major sulfur compound of Bacillus subtilis spores. J Bacteriol 98:62–68
    [Google Scholar]
  5. 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 [CrossRef]
    [Google Scholar]
  6. Brüggemann C., Denger K., Cook A. M., Ruff J. 2004; Enzymes and genes of taurine and isethionate dissimilation in Paracoccus denitrificans. Microbiology 150:805–816 [CrossRef]
    [Google Scholar]
  7. Consden R., Gordon A. H., Martin A. J. P. 1946; The identification of amino-acids derived from cysteine in chemically modified wool. Biochem J 40:580–582
    [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. Denger K., Cook A. M. 2001; Ethanedisulfonate is degraded via sulfoacetaldehyde in Ralstonia sp. strain EDS1. Arch Microbiol 176:89–95 [CrossRef]
    [Google Scholar]
  10. 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]
  11. 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]
  12. Denger K., Weinitschke S., Hollemeyer K., Cook A. M. 2004; Sulfoacetate generated by Rhodopseudomonas palustris from taurine. Arch Microbiol 182:254–258
    [Google Scholar]
  13. Dreyer J. L. 1987; The role of iron in the activation of mannonic and altronic acid hydratases, two Fe-requiring hydro-lyases. Eur J Biochem 166:623–630 [CrossRef]
    [Google Scholar]
  14. González J. M., Covert J. S., Whitman W. B. 8 other authors & ; 2003; Silicibacter pomeroyi sp.nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int J Syst Evol Microbiol 53:1261–1269 [CrossRef]
    [Google Scholar]
  15. Goris J., Vos P. D., Caballero-Mellado J., Park J., Falsen E., Quensen J. F. I., Tiedje J. M., Vandamme P. 2004; Classification of the PCB- and biphenyl-degrading strain LB400 and relatives as Burkholderia xenovorans sp. nov. Int J Syst Evol Microbiol 54:1677–1681 [CrossRef]
    [Google Scholar]
  16. Graham D. E., White R. H. 2002; Elucidation of methanogenic coenzyme biosyntheses: from spectroscopy to genomics. Nat Prod Rep 19:133–147 [CrossRef]
    [Google Scholar]
  17. Graham D. E., Xu H., White R. H. 2002; Identification of coenzyme M biosynthetic phosphosulfolactate synthase: a new family of sulfonate biosynthesizing enzymes. J Biol Chem 277:13421–13429 [CrossRef]
    [Google Scholar]
  18. Graupner M., Xu H., White R. H. 2000a; Identification of the gene encoding sulfopyruvate decarboxylase, an enzyme involved in biosynthesis of coenzyme M. J Bacteriol 182:4862–4867 [CrossRef]
    [Google Scholar]
  19. Graupner M., Xu H., White R. H. 2000b; Identification of an archaeal 2-hydroxy acid dehydrogenase catalyzing reactions involved in coenzyme biosynthesis in methanoarchaea. J Bacteriol 182:3688–3692 [CrossRef]
    [Google Scholar]
  20. Gulick A. M., Palmer D. R., Babbitt P. C., Gerlt J. A., Rayment I. 1998; Evolution of enzymatic activities in the enolase superfamily: crystal structure of (D)-glucarate dehydratase fromPseudomonas putida . Biochemistry 37:14358–14368 [CrossRef]
    [Google Scholar]
  21. Homolya L., Varadi A., Sarkadi B. 2003; Multidrug resistance-associated proteins: export pumps for conjugates with glutathione, glucuronate or sulfate. Biofactors 17:103–114 [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. Kennedy S. I. T., Fewson C. A. 1968; Enzymes of the mandelate pathway in bacterium N.C.I.B. 8250. Biochem J 107:497–506
    [Google Scholar]
  24. Kung C., Blount P. 2004; Channels in microbes: so many holes to fill. Mol Microbiol 53:373–380 [CrossRef]
    [Google Scholar]
  25. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
    [Google Scholar]
  26. Lamprecht W., Heinz F. 1984; Pyruvate. In Methods of Enzymatic Analysis pp 570–577 Edited by Bergmeyer H. U. Weinheim: Verlag Chemie;
    [Google Scholar]
  27. 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 [CrossRef]
    [Google Scholar]
  28. Laue H., Denger K., Cook A. M. 1997a; Taurine reduction in anaerobic respiration of Bilophila wadsworthia RZATAU. Appl Environ Microbiol 63:2016–2021
    [Google Scholar]
  29. Laue H., Denger K., Cook A. M. 1997b; Fermentation of cysteate by a sulfate-reducing bacterium. Arch Microbiol 168:210–214 [CrossRef]
    [Google Scholar]
  30. Lie T. J., Pitta T., Leadbetter E. R., Godchaux W., Leadbetter J. R. III 1996; Sulfonates: novel electron acceptors in anaerobic respiration. Arch Microbiol 166:204–210 [CrossRef]
    [Google Scholar]
  31. 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]
  32. Lie T. J., Godchaux W., Leadbetter E. R. 1999; Sulfonates as terminal electron acceptors for growth of sulfite-reducing bacteria (Desulfitobacterium spp.) and sulfate-reducing bacteria: effects of inhibitors of sulfidogenesis. Appl Environ Microbiol 65:4611–4617
    [Google Scholar]
  33. Mikosch C., Denger K., Cook A. M, Schäfer E.-M. 1999; Anaerobic oxidations of cysteate: degradation via a cysteate: 2-oxoglutarate aminotransferase in Paracoccus pantotrophus. Microbiology 145:1153–1160 [CrossRef]
    [Google Scholar]
  34. Pardee A. B., Prestidge L. S., Whipple M. B., Dreyfuss J. 1966; A binding site for sulfate and its relation to sulfate transport into Salmonella typhimurium . J Biol Chem 241:3962–3969
    [Google Scholar]
  35. 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]
  36. Roy A. B., Hewlins M. J. E., Ellis A. J., Harwood J. L., White G. F. 2003; Glycolytic breakdown of sulfoquinovose in bacteria: a missing link in the sulfur cycle. Appl Environ Microbiol 69:6434–6441 [CrossRef]
    [Google Scholar]
  37. 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]
  38. Sanger F. 1945; The free amino groups of insulin. Biochem J 39:507–515
    [Google Scholar]
  39. Schläfli H. R., Weiss M. A., Leisinger T., Cook A. M. 1994; Terephthalate 1,2-dioxygenase system from Comamonas testosteroni T-2: purification and some properties of the oxygenase component. J Bacteriol 176:6644–6652
    [Google Scholar]
  40. Schleheck D., Dong W., Denger K., Heinzle E., Cook A. M. 2000; An α-proteobacterium converts linear alkylbenzenesulfonate (LAS) surfactants into sulfophenylcarboxylates, and linear alkyldiphenyletherdisulfonate surfactants into sulfodiphenylethercarboxylates. Appl Environ Microbiol 66:1911–1916 [CrossRef]
    [Google Scholar]
  41. Schmidt E. 1974; Glutamat-dehydrogenase UV-test. In Methoden der Enzymatischen Analyse pp 689–696 Edited by Bergmeyer H. U. Weinheim: Verlag Chemie;
    [Google Scholar]
  42. Schomburg D., Schomburg I., Chang A. 2002; Lyases II: EC 4.1.3–4.2.1. In Springer Handbook of Enzymes Edited by Schomburg D., Schomburg I. Berlin: Springer;
    [Google Scholar]
  43. Sörbo B. 1987; Sulfate: turbidimetric and nephelometric methods. Methods Enzymol 143:3–6
    [Google Scholar]
  44. Stapley E. O., Starkey R. L. 1970; Decomposition of cysteic acid and taurine by soil microorganisms. J Gen Microbiol 64:77–84 [CrossRef]
    [Google Scholar]
  45. 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]
  46. Tralau T., Cook A. M., Ruff J. 2003a; An additional regulator, TsaQ, is involved with TsaR in regulation of transport during the degradation of p-toluenesulfonate in Comamonas testosteroni T-2. Arch Microbiol 180:319–326 [CrossRef]
    [Google Scholar]
  47. Tralau T., Mampel J., Cook A. M., Ruff J. 2003b; Characterization of TsaR, an oxygen-sensitive LysR-type regulator for the degradation of p-toluenesulfonate in Comamonas testosteroni T-2. Appl Environ Microbiol 69:2298–2305 [CrossRef]
    [Google Scholar]
  48. Vandamme P., Coenye T. 2004; Taxonomy of the genus Cupriavidus: a tale of lost and found. Int J Syst Evol Microbiol 54:2285–2289 [CrossRef]
    [Google Scholar]
  49. Venter J. C., Remington K., Heidelberg J. F. & 20 other authors; 2004; Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74 [CrossRef]
    [Google Scholar]
  50. Vollrath F., Fairbrother W. J., Williams R. J. P., Tillinghast E. K., Bernstein D. T., Gallagher K. S., Townley M. A. 1990; Compounds in the droplets of the orb spider's viscid spiral. Nature 345:526–528 [CrossRef]
    [Google Scholar]
  51. Weinstein C. L., Griffith O. W. 1986; β-Sulfopyruvate: chemical and enzymatic syntheses and enzymatic assay. Anal Biochem 156:154–160 [CrossRef]
    [Google Scholar]
  52. Weinstein C. L., Griffith O. W. 1988; Cysteinesulfonate and β-sulfopyruvate metabolism. Partitioning between decarboxylation, transamination, and reduction pathways. J Biol Chem 263:3735–3743
    [Google Scholar]
  53. White R. H. 1984; Biosynthesis of the sulfonolipid 2-amino-3-hydroxy-15-methylhexadecane-1-sulfonic acid in the gliding bacterium Cytophaga johnsonae . J Bacteriol 159:42–46
    [Google Scholar]
  54. White R. H. 1986; Intermediates in the biosynthesis of coenzyme M (2-mercaptoethanesulfonic acid. Biochemistry 25:5304–5308 [CrossRef]
    [Google Scholar]
  55. Widdel F., Pfennig N. 1981; Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids. I. Isolation of new sulfate-reducing bacteria enriched with acetate from saline environments. Description of Desulfobacter postgatei gen. nov., sp. nov. Arch Microbiol 129:395–400 [CrossRef]
    [Google Scholar]
  56. Wood D. A. 1971; Sporulation in Bacillus subtilis. The appearance of sulpholactic acid as a marker event for sporulation. Biochem J 123:601–605
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27548-0
Loading
/content/journal/micro/10.1099/mic.0.27548-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed