1887

Abstract

A degradative pathway for taurine (2-aminoethanesulfonate) in 2.4.1 was proposed by Brüggemann . (2004) ( , 805–816) on the basis of a partial genome sequence. In the present study, 2.4.1 was found to grow exponentially with taurine as the sole source of carbon and energy for growth. When taurine was the sole source of nitrogen in succinate-salts medium, the taurine was rapidly degraded, and most of the organic nitrogen was excreted as the ammonium ion, which was then utilized for growth. Most of the enzymes involved in dissimilation, taurine dehydrogenase (TDH), sulfoacetaldehyde acetyltransferase (Xsc) and phosphate acetyltransferase (Pta), were found to be inducible, and evidence for transcription of the corresponding genes (, and ), as well as of , encoding the postulated TRAP transporter for taurine, and of , encoding the sulfate exporter, was obtained by reverse-transcription PCR. An additional branch of the pathway, observed by Novak . (2004) ( , 1881–1891) in TAU3, involves taurine : pyruvate aminotransferase (Tpa) and a presumptive ABC transporter (NsbABC). No evidence for a significant role of this pathway, or of the corresponding alanine dehydrogenase (Ald), was obtained for 2.4.1. The anaplerotic pathway needed under these conditions in 2.4.1 seems to involve malyl-CoA lyase, which was synthesized inducibly, and not malate synthase (GlcB), whose presumed gene was not transcribed under these conditions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.29195-0
2006-11-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/11/3197.html?itemId=/content/journal/micro/10.1099/mic.0.29195-0&mimeType=html&fmt=ahah

References

  1. Abraham, W.-R., Strömpl, C., Vancanneyt, M., Bennasar, A., Swings, J., Lünsdorf, H., Smit, J. & Moore, E. R. B. ( 2004; ). Woodsholea maritima gen. nov., sp. nov., a marine bacterium with a low diversity of polar lipids. Int J Syst Evol Microbiol 54, 1227–1234.[CrossRef]
    [Google Scholar]
  2. Alber, B. E., Spanheimer, R., Ebenau-Jehle, C. & Fuchs, G. ( 2006; ). Study of an alternative glyoxylate cycle for acetate assimilation by Rhodobacter sphaeroides. Mol Microbiol 61, 297–309.[CrossRef]
    [Google Scholar]
  3. Allen, J. A. & Garrett, M. R. ( 1971; ). Taurine in marine invertebrates. Adv Mar Biol 9, 205–253.[CrossRef]
    [Google Scholar]
  4. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. ( 1997; ). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402.[CrossRef]
    [Google Scholar]
  5. Bergmeyer, H. U., Graßl, M. & Walter, E.-M. ( 1983; ). Phosphotransacetylase. In Methods of Enzymatic Analysis, pp. 295–296. Edited by H. U. Bergmeyer. Weinheim: Verlag Chemie.
  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.[CrossRef]
    [Google Scholar]
  7. 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]
  8. Cook, A. M. ( 1987; ). Biodegradation of s-triazine xenobiotics. FEMS Microbiol Rev 46, 93–116.[CrossRef]
    [Google Scholar]
  9. Cook, A. M. & Hütter, R. ( 1981; ). s-Triazines as nitrogen sources for bacteria. J Agric Food Chem 29, 1135–1143.[CrossRef]
    [Google Scholar]
  10. Cook, A. M. & Denger, K. ( 2002; ). Dissimilation of the C2 sulfonates. Arch Microbiol 179, 1–6.[CrossRef]
    [Google Scholar]
  11. Cook, A. M. & Denger, K. ( 2006; ). Metabolism of taurine in microorganisms: a primer in molecular diversity? Adv Exp Med Biol 583, 3–13.
    [Google Scholar]
  12. 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]
  13. 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.[CrossRef]
    [Google Scholar]
  14. Denger, K., Ruff, J., Schleheck, D. & Cook, A. M. ( 2004a; ). Rhodococcus opacus expresses the xsc gene to utilize taurine as a carbon source or as a nitrogen source but not as a sulfur source. Microbiology 150, 1859–1867.[CrossRef]
    [Google Scholar]
  15. Denger, K., Weinitschke, S., Hollemeyer, K. & Cook, A. M. ( 2004b; ). Sulfoacetate generated by Rhodopseudomonas palustris from taurine. Arch Microbiol 182, 254–258.
    [Google Scholar]
  16. Denger, K., Smits, T. H. M. & Cook, A. M. ( 2006; ). l-Cysteate sulfo-lyase, a widespread, pyridoxal 5′-phosphate-coupled desulfonative enzyme purified from Silicibacter pomeroyi DSS-3T. Biochem J 394, 657–664.[CrossRef]
    [Google Scholar]
  17. Desomer, J., Crespi, M. & Van Montagu, M. ( 1991; ). Illegitimate integration of non-replicative vectors in the genome of Rhodococcus fascians upon electrotransformation as an insertional mutagenesis system. Mol Microbiol 5, 2115–2124.[CrossRef]
    [Google Scholar]
  18. Dixon, G. H. & Kornberg, H. L. ( 1959; ). Assay methods for key enzymes of the glyoxylate cycle. Biochem J 72, 3P.
    [Google Scholar]
  19. Eichhorn, E., van der Ploeg, J. R. & Leisinger, T. ( 2000; ). Deletion analysis of the Escherichia coli taurine and alkanesulfonate transport systems. J Bacteriol 182, 2687–2795.[CrossRef]
    [Google Scholar]
  20. Filatova, L. V., Berg, I. A., Krasil'nikova, E. N. & Ivanovsky, R. N. ( 2005; ). A study of the mechanism of acetate assimilation in purple nonsulfur bacteria lacking the glyoxylate shunt: enzymes of the citramalate cycle in Rhodobacter sphaeroides. Microbiology (English translation of Mikrobiologiia) 74, 270–278.[CrossRef]
    [Google Scholar]
  21. Forward, J. A., Behrendt, M. C., Wyborn, N. R., Cross, R. & Kelly, D. J. ( 1997; ). TRAP transporters: a new family of periplasmic solute transport systems encoded by the dctPQM genes of Rhodobacter capsulatus and by homologs in diverse gram-negative bacteria. J Bacteriol 179, 5482–5493.
    [Google Scholar]
  22. Gesellschaft Deutscher Chemiker ( 1996; ). German Standard Methods for the Laboratory Examination of Water, Waste Water and Sludge. Weinheim: Verlag Chemie.
  23. 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, 402–606.[CrossRef]
    [Google Scholar]
  24. Hagen, K. D. & Nelson, D. C. ( 1997; ). Use of reduced sulfur compounds by Beggiatoa spp.: enzymology and physiology of marine and freshwater strains in homogeneous and gradient cultures. Appl Environ Microbiol 63, 3957–3964.
    [Google Scholar]
  25. Huxtable, R. J. ( 1992; ). Physiological actions of taurine. Physiol Rev 72, 101–163.
    [Google Scholar]
  26. 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.
  27. Kappler, U. & Dahl, C. ( 2001; ). Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol Lett 203, 1–9.[CrossRef]
    [Google Scholar]
  28. 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.[CrossRef]
    [Google Scholar]
  29. 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]
  30. Khademi, S., O'Connell, J., III, Remis, J., Robles-Colmenares, Y., Miercke, L. J. & Stroud, R. M. ( 2004; ). Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å. Science 305, 1587–1594.[CrossRef]
    [Google Scholar]
  31. Kinhikar, A. G., Vargas, D., Li, H., Mahaffey, S. B., Hinds, L., Belisle, J. T. & Laal, S. ( 2006; ). Mycobacterium tuberculosis malate synthase is a laminin-binding adhesin. Mol Microbiol 60, 999–1013.[CrossRef]
    [Google Scholar]
  32. Laemmli, U. K. ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.[CrossRef]
    [Google Scholar]
  33. Laue, H. & Cook, A. M. ( 2000a; ). Purification, properties and primary structure of alanine dehydrogenase involved in taurine metabolism in the anaerobe Bilophila wadsworthia. Arch Microbiol 174, 162–167.[CrossRef]
    [Google Scholar]
  34. Laue, H. & Cook, A. M. ( 2000b; ). Biochemical and molecular characterization of taurine : pyruvate aminotransferase from the anaerobe Bilophila wadsworthia. Eur J Biochem 267, 6841–6848.[CrossRef]
    [Google Scholar]
  35. Laue, H., Smits, T. H. M., Schumacher, U., Claros, M., Hartemink, R. & Cook, A. M. ( 2006; ). Identification of Bilophila wadsworthia in enrichment cultures by specific PCR which targets the taurine : pyruvate aminotransferase gene. FEMS Microbiol Lett 261, 74–79.[CrossRef]
    [Google Scholar]
  36. Lawrence, S. H., Luther, K. B., Schindelin, H. & Ferry, J. G. ( 2006; ). Structural and functional studies suggest a catalytic mechanism for the phosphotransacetylase from Methanosarcina thermophila. J Bacteriol 188, 1143–1154.[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. Masepohl, B., Führer, F. & Klipp, W. ( 2001; ). Genetic analysis of a Rhodobacter capsulatus gene region involved in utilization of taurine as a sulfur source. FEMS Microbiol Lett 205, 105–111.[CrossRef]
    [Google Scholar]
  39. 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.[CrossRef]
    [Google Scholar]
  40. Meister, M., Saum, S., Alber, B. E. & Fuchs, G. ( 2005; ). l-Malyl-coenzyme A/β-methylmalyl-coenzyme A lyase is involved in acetate assimilation of the isocitrate lyase-negative bacterium Rhodobacter capsulatus. J Bacteriol 187, 1415–1425.[CrossRef]
    [Google Scholar]
  41. Novak, R. T., Gritzer, R. F., Leadbetter, E. R. & Godchaux, W. ( 2004; ). Phototrophic utilization of taurine by the purple nonsulfur bacteria Rhodopseudomonas palustris and Rhodobacter sphaeroides. Microbiology 150, 1881–1891.[CrossRef]
    [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., Gueta, R., Denger, K., Ruff, J., Hollemeyer, K. & Cook, A. M. ( 2005; ). Dissimilation of cysteate via 3-sulfolactate sulfo-lyase and a sulfate exporter in Paracoccus pantotrophus NKNCYSA. Microbiology 151, 737–747.[CrossRef]
    [Google Scholar]
  44. 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]
  45. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor: Cold Spring Harbor Laboratory.
  46. Schiffer, A., Fritz, G., Kroneck, P. M. & 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.[CrossRef]
    [Google Scholar]
  47. Sistrom, W. R. ( 1962; ). The kinetics of the synthesis of photopigments in Rhodopseudomonas sphaeroides. J Gen Microbiol 28, 607–616.[CrossRef]
    [Google Scholar]
  48. Sörbo, B. ( 1987; ). Sulfate: turbidimetric and nephelometric methods. Methods Enzymol 143, 3–6.
    [Google Scholar]
  49. Styp von Rekowski, K., Denger, K. & Cook, A. M. ( 2005; ). Isethionate as a product from taurine during nitrogen-limited growth of Klebsiella oxytoca Tau-N1. Arch Microbiol 183, 325–330.[CrossRef]
    [Google Scholar]
  50. Thurnheer, T., Köhler, T., Cook, A. M. & Leisinger, T. ( 1986; ). Orthanilic acid and analogues as carbon sources for bacteria: growth physiology and enzymic desulphonation. J Gen Microbiol 132, 1215–1220.
    [Google Scholar]
  51. 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]
  52. 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.[CrossRef]
    [Google Scholar]
  53. Weinitschke, S., Denger, K., Smits, T. H. M., Hollemeyer, K. & Cook, A. M. ( 2006; ). The sulfonated osmolyte N-methyltaurine is dissimilated by Alcaligenes faecalis and by Paracoccus versutus with release of methylamine. Microbiology 152, 1179–1186.[CrossRef]
    [Google Scholar]
  54. 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]
  55. Yin, M., Palmer, H. R., Fyfe-Johnson, A. L., Bedford, J. J., Smith, R. A. & Yancey, P. H. ( 2000; ). Hypotaurine, N-methyltaurine, taurine, and glycine betaine as dominant osmolytes of vestimentiferan tubeworms from hydrothermal vents and cold seeps. Physiol Biochem Zool 73, 629–637.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.29195-0
Loading
/content/journal/micro/10.1099/mic.0.29195-0
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