1887

Abstract

Selective enrichments yielded bacterial cultures able to utilize the osmolyte -methyltaurine as sole source of carbon and energy or as sole source of fixed nitrogen for aerobic growth. Strain MT1, which degraded -methyltaurine as a sole source of carbon concomitantly with growth, was identified as a strain of . Stoichiometric amounts of methylamine, whose identity was confirmed by matrix-assisted, laser-desorption ionization time-of-flight mass spectrometry, and of sulfate were released during growth. Inducible -methyltaurine dehydrogenase, sulfoacetaldehyde acetyltransferase (Xsc) and a sulfite dehydrogenase could be detected. Taurine dehydrogenase was also present and it was hypothesized that taurine dehydrogenase has a substrate range that includes -methyltaurine. Partial sequences of a -like gene (encoding the putative large component of taurine dehydrogenase) and an gene were obtained by PCR with degenerate primers. Strain N-MT utilized -methyltaurine as a sole source of fixed nitrogen for growth and could also utilize the compound as sole source of carbon. This bacterium was identified as a strain of . This organism also expressed inducible (-methyl)taurine dehydrogenase, Xsc and a sulfite dehydrogenase. The presence of a gene cluster with high identity to a larger cluster from NKNCYSA, which is now known to dissimilate -methyltaurine via Xsc, allowed most of the overall pathway, including transport and excretion, to be defined. -Methyltaurine is thus another compound whose catabolism is channelled directly through sulfoacetaldehyde.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28622-0
2006-04-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/4/1179.html?itemId=/content/journal/micro/10.1099/mic.0.28622-0&mimeType=html&fmt=ahah

References

  1. Allen, J. A. & Garrett, M. R. ( 1971; ). Taurine in marine invertebrates. Adv Mar Biol 9, 205–253.[CrossRef]
    [Google Scholar]
  2. 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]
  3. Baker, S. C., Ferguson, S. J., Ludwig, B., Page, M. D., Richter, O.-M. H. & van Spanning, R. J. M. ( 1998; ). Molecular genetics of the genus Paracoccus: metabolically versatile bacteria with bioenergetic flexibility. Microbiol Mol Biol Rev 62, 1046–1078.
    [Google Scholar]
  4. 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.
  5. Booth, I. R., Edwards, M. D., Murray, E. & Miller, S. ( 2005; ). The role of bacterial channels in cell physiology. In Bacterial Ion Channels and their Eukaryotic Homologs, pp. 291–312. Edited by A. Kubalski & B. Martinac. Washington, DC: American Society for Microbiology.
  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. Cook, A. M. ( 1987; ). Biodegradation of s-triazine xenobiotics. FEMS Microbiol Rev 46, 93–116.[CrossRef]
    [Google Scholar]
  8. Cook, A. M. & Denger, K. ( 2002; ). Dissimilation of the C2 sulfonates. Arch Microbiol 179, 1–6.[CrossRef]
    [Google Scholar]
  9. 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]
  10. Cook, A. M. & Hütter, R. ( 1981; ). s-Triazines as nitrogen sources for bacteria. J Agric Food Chem 29, 1135–1143.[CrossRef]
    [Google Scholar]
  11. 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]
  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 sequence. Biochem J 357, 581–586.[CrossRef]
    [Google Scholar]
  13. 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]
  14. Denger, K., Weinitschke, S., Hollemeyer, K. & Cook, A. M. ( 2004b; ). Sulfoacetate generated by Rhodopseudomonas palustris from taurine. Arch Microbiol 182, 254–258.
    [Google Scholar]
  15. 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 (in press). doi:10.1042/BJ20051311
    [Google Scholar]
  16. 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]
  17. Eady, R. R. & Large, P. J. ( 1968; ). Purification and properties of an amine dehydrogenase from Pseudomonas AM1 and its role in growth on methylamine. Biochem J 106, 245–255.
    [Google Scholar]
  18. 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]
  19. Gerhardt, P., Murray, R. G. E., Wood, W. A. & Krieg, N. R. ( 1994; ). .Methods for General and Molecular Bacteriology. Washington, DC: American Society for Microbiology.
  20. Gesellschaft Deutscher Chemiker ( 1996; ). German Standard Methods for the Laboratory Examination of Water, Waste Water and Sludge. Weinheim: Verlag Chemie.
  21. 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]
  22. Holt, J. G., Krieg, N. R., Sneath, P. H. A., Staley, J. T. & Williams, S. T. ( 1994; ). Bergey's Manual of Determinative Bacteriology, 9th edn. Baltimore: Williams & Wilkins.
  23. Huxtable, R. J. ( 1992; ). Physiological actions of taurine. Physiol Rev 72, 101–163.
    [Google Scholar]
  24. Jones, K. M. ( 1979; ). Artificial substrates and biochemical reagents. In Data for Biochemical Research, pp. 436–465. Edited by R. M. C. Dawson, D. C. Elliott, W. H. Elliott & K. M. Jones. Oxford: Oxford University Press.
  25. 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]
  26. Kelly, D. P., McDonald, I. R. & Wood, A. P. ( 2000; ). Proposal for the reclassification of Thiobacillus novellus as Starkeya novella gen. nov., comb. nov., in the α-subclass of the Proteobacteria. Int J Syst Evol Microbiol 50, 1797–1802.
    [Google Scholar]
  27. 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]
  28. Khademi, S., O'Connell, J., 3rd, 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]
  29. Lang, E. & Lang, H. ( 1972; ). Spezifische Farbreaktionen zum direkten Nachweis der Ameisensäure. Z Anal Chem 260, 8–10.[CrossRef]
    [Google Scholar]
  30. Laue, H. & Cook, A. M. ( 2000; ). 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]
  31. 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]
  32. Mampel, J., Maier, E., Tralau, T., Ruff, J., Benz, R. & Cook, A. M. ( 2004; ). A novel outer-membrane anion channel (porin) as part of the putatively two-component transport system for p-toluenesulfonate in Comamonas testosteroni T-2. Biochem J 383, 91–99.[CrossRef]
    [Google Scholar]
  33. Martinez, B., Tomkins, J., Wackett, L. P., Wing, R. & Sadowsky, M. J. ( 2001; ). Complete nucleotide sequence and organization of the atrazine catabolic plasmid pADP-1 from Pseudomonas sp. strain ADP. J Bacteriol 183, 5684–5697.[CrossRef]
    [Google Scholar]
  34. Moore, E. R. B., Mau, M., Arnscheidt, A., Bottger, E. C., Hutson, R. A., Collins, M. D., VandePeer, Y., DeWachter, R. & Timmis, K. N. ( 1996; ). The determination and comparison of the 16S rRNA gene sequences of species of the genus Pseudomonas (sensu stricto) and estimation of the natural intrageneric relationships. Syst Appl Microbiol 19, 478–492.[CrossRef]
    [Google Scholar]
  35. 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]
  36. Rainey, F., Kelly, D. P., Stackebrandt, E., Burkhardt, J., Hiraishi, A., Katayama, Y. & Wood, A. P. ( 1999; ). A reevaluation of the taxonomy of Paracoccus denitrificans and a proposal for the creation of Paracoccus pantotrophus comb. nov. Int J Syst Bacteriol 49, 645–651.[CrossRef]
    [Google Scholar]
  37. Regeard, C., Maillard, J. & Holliger, C. ( 2004; ). Development of degenerate and specific PCR primers for the detection and isolation of known and putative chloroethene reductive dehalogenase genes. J Microbiol Methods 56, 107–118.[CrossRef]
    [Google Scholar]
  38. 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]
  39. 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]
  40. 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]
  41. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  42. Smits, T. H. M., Röthlisberger, M., Witholt, B. & van Beilen, J. B. ( 1999; ). Molecular screening for alkane hydroxylase genes in Gram-negative and Gram-positive strains. Environ Microbiol 1, 307–317.[CrossRef]
    [Google Scholar]
  43. Sörbo, B. ( 1987; ). Sulfate: turbidimetric and nephelometric methods. Methods Enzymol 143, 3–6.
    [Google Scholar]
  44. Stipanuk, M. H. ( 2004; ). Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. Annu Rev Nutr 24, 539–577.[CrossRef]
    [Google Scholar]
  45. Takagi, K., Torimura, M., Kawaguchi, K., Kano, K. & Ikeda, T. ( 1999; ). Biochemical and electrochemical characterization of quinohemoprotein amine dehydrogenase from Paracoccus denitrificans. Biochemistry 38, 6935–6942.[CrossRef]
    [Google Scholar]
  46. 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]
  47. 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]
  48. van Beilen, J. B., Mourlane, F., Seeger, M. A., Kovac, J., Li, Z., Smits, T. H. M., Fritsche, U. & Witholt, B. ( 2003; ). Cloning of Baeyer-Villiger monooxygenases from Comamonas, Xanthobacter and Rhodococcus using polymerase chain reaction with highly degenerate primers. Environ Microbiol 5, 174–182.[CrossRef]
    [Google Scholar]
  49. 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]
  50. 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]
  51. Wilson, M. M. & Metcalf, W. W. ( 2005; ). Genetic diversity and horizontal transfer of genes involved in oxidation of reduced phosphorus compounds by Alcaligenes faecalis WM2072. Appl Environ Microbiol 71, 290–296.[CrossRef]
    [Google Scholar]
  52. Yancey, P. H., Blake, W. R. & Conley, J. ( 2002; ). Unusual organic osmolytes in deep-sea animals: adaptations to hydrostatic pressure and other perturbants. Comp Biochem Physiol A Mol Integr Physiol 133, 667–676.[CrossRef]
    [Google Scholar]
  53. 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.0.28622-0
Loading
/content/journal/micro/10.1099/mic.0.28622-0
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