1887

Abstract

Taurine metabolism by two phototrophically grown purple nonsulfur bacteria enrichment isolates has been examined. (strain Tau1) grows with taurine as a sole electron donor, sulfur and nitrogen source during photoautotrophic growth. (strain Tau3) grows on the compound as sole electron donor, sulfur and nitrogen source, and partial carbon source, in the presence of CO during photoheterotrophic growth. Both organisms utilize an inducible taurine–pyruvate aminotransferase and a sulfoacetaldehyde acetyltransferase. The products of this metabolism are bisulfite and acetyl phosphate. Bisulfite ultimately was oxidized to sulfate, but this was not an adequate source of electrons for photometabolism. Experiments using either [U-C]taurine or CO demonstrated that Tau3 assimilated the carbon from approximately equimolar amounts of taurine and exogenous CO. The taurine-carbon assimilation was not diminished by excess non-radioactive bicarbonate. Malate synthase (but not isocitrate lyase) was induced in these taurine-grown cells. It is concluded that assimilation of taurine carbon occurs through an intermediate other than CO. Similar labelling experiments with Tau1 determined that taurine is utilized only as an electron donor for the reduction of CO, which contributes all the cell carbon. Photoautotrophic metabolism was confirmed in this organism by the absence of either malate synthase or isocitrate lyase in taurine+CO-grown cells. Culture collection strains of these two bacteria did not utilize taurine in these fashions.

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2004-06-01
2019-12-12
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References

  1. Albers, H. & Gottschalk, G. ( 1976; ). Acetate metabolism in Rhodopseudomonas gelatinosa and several other Rhodospirillaceae. Arch Microbiol 111, 45–49.[CrossRef]
    [Google Scholar]
  2. Barbosa, M. J., Rocha, J. M. S., Tramper, J. & Wijffels, R. H. ( 2001; ). Acetate as a carbon source for hydrogen production by photosynthetic bacteria. J Biotechnol 85, 25–33.[CrossRef]
    [Google Scholar]
  3. Benyajati, S. & Renfro, J. L. ( 2000; ). Taurine secretion in primary monolayer cultures of flounder renal epithelium: stimulation by low osmolality. Am J Physiol Regul Integr Comp Physiol 279, 704–712.
    [Google Scholar]
  4. Berg, I. A., Filatova, L. V. & Ivanovsky, R. N. ( 2002; ). Inhibition of acetate and propionate assimilation by itaconate via propionyl-CoA carboxylase in isocitrate lyase-negative purple bacterium Rhodospirillum rubrum. FEMS Microbiol Lett 216, 49–54.[CrossRef]
    [Google Scholar]
  5. Brune, A., Miambi, E. & Breznak, J. ( 1995; ). Roles of oxygen and the intestinal microflora in the metabolism of lignin-derived phenylpropanoids and other monoaromatic compounds by termites. Appl Environ Microbiol 61, 2688–2695.
    [Google Scholar]
  6. Burton, R. S. & Feldman, M. W. ( 1982; ). Changes in free amino acid concentrations during osmotic response in the intertidal copepod Tigriopus californicus. Comp Biochem Physiol 73, 441–445.[CrossRef]
    [Google Scholar]
  7. Chien, C.-C., Leadbetter, E. R. & Godchaux, W., III ( 1995; ). Sulfonate-sulfur can be assimilated for fermentative growth. FEMS Microbiol Lett 129, 189–194.[CrossRef]
    [Google Scholar]
  8. Chien, C.-C., Leadbetter, E. R. & Godchaux, W., III ( 1997; ). Taurine-sulfur assimilation and taurine-pyruvate aminotransferase activity in anaerobic bacteria. Appl Environ Microbiol 63, 3021–3024.
    [Google Scholar]
  9. Chien, C.-C., Leadbetter, E. R. & Godchaux, W., III ( 1999; ). Rhodococcus spp. utilize taurine (2-aminoethanesulfonate) as sole source of carbon, energy, nitrogen and sulfur for aerobic respiratory growth. FEMS Microbiol Lett 176, 333–337.[CrossRef]
    [Google Scholar]
  10. Cohen-Bazire, G., Sistrom, W. R. & Stanier, R. Y. ( 1957; ). Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J Cell Comp Physiol 49, 25–68.[CrossRef]
    [Google Scholar]
  11. Denger, K., Kertesz, M., Vock, E., Schöon, R., Mägli, A. & Cook, A. ( 1996; ). Anaerobic desulfonation of 4-tolylsulfonate and 2-(4-sulfophenyl) butyrate by a Clostridium sp. Appl Environ Microbiol 62, 1526–1530.
    [Google Scholar]
  12. Denger, K., Laue, H. & Cook, A. ( 1997a; ). Anaerobic taurine oxidation: a novel reaction by a nitrate-reducing Alcaligenes sp. Microbiology 143, 1919–1924.[CrossRef]
    [Google Scholar]
  13. Denger, K., Laue, H. & Cook, A. M. ( 1997b; ). Thiosulfate as a metabolic product: the bacterial fermentation of taurine. Arch Microbiol 168, 297–301.[CrossRef]
    [Google Scholar]
  14. Denger, K., Ruff, J., Rein, U. & Cook, A. M. ( 2001; ). Sulphoacetaldehyde sulpho-lyase (EC 4.4.1.12) from Desulfonispora thiosulfatigenes: purification, properties and primary sequence. Biochem J 357, 581–586.[CrossRef]
    [Google Scholar]
  15. Dewhirst, F. E., Chien, C.-C., Paster, B. J., Ericson, R. L., Orcutt, R. P., Schauer, D. B. & Fox, J. G. ( 1999; ). Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl Environ Microbiol 65, 3287–3292.
    [Google Scholar]
  16. Dixon, G. H. & Kornberg, H. L. ( 1959; ). Assay methods for key enzymes of the glyoxylate cycle. Biochem J 72, 3P.
    [Google Scholar]
  17. Dutton, P. L. & Evans, W. C. ( 1969; ). The metabolism of aromatic compounds by Rhodopseudomonas palustris. Biochem J 113, 525–535.
    [Google Scholar]
  18. Dutton, P. L. & Evans, W. C. ( 1978; ). Metabolism of aromatic compounds by Rhodospirillaceae. In The Photosynthetic Bacteria, pp. 719–726. Edited by R. K. Clayton & W. R. Sistrom. New York: Plenum.
  19. Gritzer, R. F., Moffitt, K., Godchaux, W. & Leadbetter, E. R. ( 2003; ). Sulfoacetaldehyde bisulfite adduct is a substrate for enzymes presumed to act on sulfoacetaldehyde. J Microbiol Methods 53, 423–425.[CrossRef]
    [Google Scholar]
  20. Harwood, C. S. & Gibson, J. ( 1986; ). Uptake of benzoate by Rhodopseudomonas palustris grown anaerobically in light. J Bacteriol 165, 504–509.
    [Google Scholar]
  21. Harwood, C. S. & Gibson, J. ( 1988; ). Anaerobic and aerobic metabolism of diverse aromatic compounds by the photosynthetic bacterium Rhodopseudomonas palustris. Appl Environ Microbiol 54, 712–717.
    [Google Scholar]
  22. Imhoff, J. F. & Trüper, H. G. ( 1992; ). The genus Rhodospirillum and related genera. In The Prokaryotes, pp. 2141–2152. Edited by A. Balows, H. G. Truper, M. Dworkin, W. Harder & K. H. Schleifer. New York: Springer.
  23. Jackson, A. E., Ayer, S. W. & Laycock, M. V. ( 1992; ). The effect of salinity on growth and amino acid composition in the marine diatom Nitzschia pungens. Can J Bot 70, 2198–2201.[CrossRef]
    [Google Scholar]
  24. Joint Genome Institute, D. O. E. ( 2003; ). http://www.jgi.doe.gov/JGI_microbial/html/index.html. Department of Energy's Joint Genome Institute. Accessed 16 October 2003.
  25. 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]
  26. Kobayashi, M. & Nakanishi, M. ( 1971; ). Construction of a purification plant for polluted water using photosynthetic bacteria. J Ferment Technol 49, 817–825.
    [Google Scholar]
  27. Kondo, H., Anada, H., Ohsawa, K. & Ishimoto, M. ( 1971; ). Formation of sulfoacetaldehyde from taurine in bacterial extracts. J Biochem 69, 621–623.
    [Google Scholar]
  28. Laue, H. & Cook, A. M. ( 2000; ). Biochemical and molecular characterization of taurine:pyruvate aminotransferase from the anaerobe Bilophila wadsworthia. Eur J Biochem 267, 6841–6848.[CrossRef]
    [Google Scholar]
  29. Laue, H., Denger, K. & Cook, A. M. ( 1997; ). Taurine reduction in anaerobic respiration of Bilophila wadsworthia RZATAU. Appl Environ Microbiol 166, 204–210.
    [Google Scholar]
  30. Lie, T. J., Clawson, M. L., Godchaux, W., III & Leadbetter, E. R. ( 1999; ). Sulfidogenesis from 2-aminoethanesulfonate (taurine) fermentation by a morphologically unusual sulfate-reducing bacterium, Desulforhopalus singaporensis sp. nov. Appl Environ Microbiol 65, 3328–3334.
    [Google Scholar]
  31. Madigan, M. T. & Gest, H. ( 1979; ). Growth of the photosynthetic bacterium Rhodopseudomonas capsulata chemoautotrophically in darkness with H2 as the energy source. J Bacteriol 137, 524–530.
    [Google Scholar]
  32. Maidak, B., Cole, J., Lilburn, T. & 9 other authors ( 2000; ). The RDP (Ribosomal Database Project) continues. Nucleic Acids Res 28, 173–174.[CrossRef]
    [Google Scholar]
  33. Masepohl, B., Fuhrer, 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]
  34. Miller, T. & Wolin, M. ( 1974; ). A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Appl Environ Microbiol 27, 985–987.
    [Google Scholar]
  35. Payne, J. & Morris, J. G. ( 1969; ). Acetate utilization by Rhodopseudomonas sphaeroides. FEBS Lett 4, 52–54.[CrossRef]
    [Google Scholar]
  36. Pfennig, N. ( 1978; ). General physiology and ecology of photosynthetic bacteria. In The Photosynthetic Bacteria, pp. 3–18. Edited by R. K. Clayton & W. R. Sistrom. New York: Plenum.
  37. Pierce, S. K., Rowland-Faux, L. M. & O'Brien, S. M. ( 1992; ). Different salinity tolerance mechanisms in Atlantic and Chesapeake Bay conspecific oysters: glycine betaine and amino acid pool variations. Marine Biol 113, 107–115.[CrossRef]
    [Google Scholar]
  38. 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]
  39. Sansone, G., Cotugno, M., Cosma, I. & Zatta, P. ( 1987; ). The effect of beta-alanine on the concentration of taurine and other free amino acids during osmotic stress of Mytilus galloprovincialis. J Marine Biol 67, 111–117.[CrossRef]
    [Google Scholar]
  40. Schauder, R., Eikmanns, B., Thauer, R., Widdel, F. & Fuchs, G. ( 1986; ). Acetate oxidation to CO2 in anaerobic bacteria via a novel pathway not involving reactions of the citric acid cycle. Arch Microbiol 145, 162–172.[CrossRef]
    [Google Scholar]
  41. Seitz, A. P., Leadbetter, E. R., Godchaux, W., III ( 1993; ). Utilization of sulfonates as sole sulfur source by soil bacteria including Comamonas acidovorans. Arch Microbiol 159, 440–444.[CrossRef]
    [Google Scholar]
  42. Shimamoto, G. & Berk, R. ( 1979; ). Catabolism of taurine in Pseudomonas aeruginosa. Biochim Biophys Acta 569, 287–292.[CrossRef]
    [Google Scholar]
  43. Smith, P. K., Krohn, R. I., Hermanson, G. T. & 7 other authors ( 1985; ). Measurement of protein using bicinchoninic acid. Anal Biochem 150, 76–85.[CrossRef]
    [Google Scholar]
  44. Stadtman, E. R. ( 1957; ). Preparation and assay of acetyl phosphate. Methods Enzymol 3, 228–231.
    [Google Scholar]
  45. van Niel, C. ( 1971; ). Techniques for the enrichment, isolation, and maintenance of the photosynthetic bacteria. Methods Enzymol 23, 3–28.
    [Google Scholar]
  46. Vigenschow, H., Schwarm, H. M. & Knobloch, K. ( 1986; ). Purification and properties of an acetate kinase from Rhodopseudomonas palustris. Biol Chem Hoppe-Seyler 367, 951–956.[CrossRef]
    [Google Scholar]
  47. Visscher, P. T. & Taylor, B. F. ( 1993; ). Organic thiols as organolithotrophic substrates for growth of phototrophic bacteria. Appl Environ Microbiol 59, 93–96.
    [Google Scholar]
  48. Walther, M. ( 2002; ). Taurine in the marine hydrozoan Hydractinia echinata: stabilizer of the larval state? Comp Biochem Physiol A Comp Physiol 133, 179–190.[CrossRef]
    [Google Scholar]
  49. Yang, S. P., Zhao, C. G., Liu, R. T., Qu, Y. B. & Qian, X. M. ( 2002; ). Hydrogen photoproduction from acetate by Rhodopseudomonas palustris. Chinese Journal of Biotechnology (English translation of Sheng Wu Gong Cheng Xue Bao) 18, 486–491.
    [Google Scholar]
  50. 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]
  51. Yoshida, A. & Freese, E. ( 1965; ). Enzymatic properties of alanine dehydrogenase of Bacillus subtilis. Biochim Biophys Acta 96, 248–262.
    [Google Scholar]
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