1887

Abstract

PAO1 grew in defined synthetic medium with any of a broad variety of single sulfur sources, including sulfate, cysteine, thiocyanate, alkanesulfonates, organosulfate esters and methionine, but not with aromatic sulfonates, thiophenols or organothiocyanates or isothiocyanates. During growth with any of these compounds except sulfate, cysteine or thiocyanate, a set of 10 sulfate starvation-induced (SSI) proteins was strongly up-regulated, as observed by two-dimensional protein electrophoresis of total cell extracts. A comparable level of up-regulation was found for the hydrolytic enzyme arylsulfatase, which has previously been used as a marker enzyme for the sulfate starvation response. One of the SSI proteins was identified by N-terminal sequencing as a high-affinity periplasmic sulfate-binding protein, and another was related to thiol-specific antioxidants, but the N-terminal sequences of the other SSI proteins revealed no similarity to N-termini of proteins of known function, and they probably represent uncharacterized enzymes involved in sulfur scavenging when preferred sulfur sources are absent. To study the role that cysteine biosynthetic intermediates play in the synthesis of these proteins , we isolated mini-Tn transposon mutants of with insertions in the and genes, which encode subunits of ATP-sulfurylase and sulfite reductase, respectively. These two genes were cloned and sequenced. showed high similarity to the cognate gene in , whereas encoded a 69.3 kDa protein with two domains corresponding to the CysN and CysC proteins. Sulfate no longer repressed synthesis of the SSI proteins in mutants, but repression was restored by sulfite; in the mutant, sulfate, sulfite and sulfide all led to repression of SSI protein synthesis. This suggests that there are at least two independent corepressors of the sulfate starvation response in this species.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-144-5-1375
1998-05-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/144/5/mic-144-5-1375.html?itemId=/content/journal/micro/10.1099/00221287-144-5-1375&mimeType=html&fmt=ahah

References

  1. Adachi, T., Murooka, Y., Harada, T. (1975); Regulation of arylsulfatase synthesis by sulfur compounds in Klebsiella aero- genes.. Journal of Bacteriology 121:(1)29–35 [View Article]
    [Google Scholar]
  2. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. E., Seidman, J. G. et al. (1987) Current Protocols in Molecular Biology. New York:: Wiley;
    [Google Scholar]
  3. Autry, A. R., Fitzgerald, J. W. (1990); Sulfonate S - a major form of forest soil organic sulfur.. Biol Fertil Soils 10:50–56
    [Google Scholar]
  4. Beil, S., Kehrli, H., James, P., Staudenmann, W., Cook, A. M., Leisinger, T., Kertesz, M.A. (1995); Purification and characterization of the arylsulfatase synthesized by Pseudomonas aeruginosa PAO during growth in sulfate-free medium and cloning of the arylsulfatase gene (atsA).. European Journal of Biochemistry 229:(2)385–394 [View Article]
    [Google Scholar]
  5. Beil, S., Kertesz, M. A., Leisinger, T., Cook, A. M. (1996); The assimilation of sulfur from multiple sources and its correlation with expression of the sulfate-starvation-induced stimulon in Pseudomonas putida S-313.. Microbiology 142:(8)1989–1995 [View Article]
    [Google Scholar]
  6. Betts, P. M., Rinder, D. F., Flecker, J. R. (1979); Thiocyanate utilization by an Artbrobacter.. Canadian Journal of Microbiology 25:(11)1277–1282 [View Article]
    [Google Scholar]
  7. Boucabeille, C., Bories, A., Olivier, P., Calhoun, D. H., Feary, T. W. (1994); Degradation of thiocyanate by a bacterial coculture, Transductional analysis of Pseudomonas aeruginosa methionineless auxotrophs.. Biotechnology Letters 16:(4)425–430 [View Article]
    [Google Scholar]
  8. Cashel, M., Gentry, D. R., Hernandez, V. J., Vinella, D. (1996) The stringent response.. Edited by Neidhardt, F. C., et, al. Escherichia coli and Salmonella. Washington:: American Society for Microbiology,;1458–1496
    [Google Scholar]
  9. Chae, H. Z., Robison, K., Poole, L. B., Church, G., Storz, G., Rhee, S. G. (1994); Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol- specific antioxidant define a large family of antioxidant enzymes.. Proc Natl Acad Sci USA 91:(15)7017–7021 [View Article]
    [Google Scholar]
  10. Crane, B. R., Siegel, L. M., Getzoff, E. D. (1995); Sulfite reductase structure at T6 A: evolution and catalysis for reduction of inorganic anions.. Science 270:(5233)59–67 [View Article]
    [Google Scholar]
  11. Delic-Attree, I., Toussaint, B., Garin, J., Vignais, P. M. (1997); Cloning, sequence and mutagenesis of the structural gene of Pseudomonas aeruginosa CysB, which can activate algD transcription. Molecular Microbiology 241275–1284
    [Google Scholar]
  12. De Lorenzo, V., Timmis, K. N. (1994); Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and TnlO-derived minitransposons.. Methods in Enzymology, Vol 46: Research on Nitrification and Related Processes, Pt B 235:386–405
    [Google Scholar]
  13. Dodgson, K. S., White, G. F., Fitzgerald, J. W. (1982) Sulfatases of Microbial Origin. Boca Raton, FL:: CRC Press;
    [Google Scholar]
  14. Dudley, M. W., Frost, J. W. (1994); Biocatalytic desulfurization of arylsulfonates.. Bioorg Med Chem 2:(7)681–690 [View Article]
    [Google Scholar]
  15. Eichhorn, E., van der Ploeg, J. R., Kertesz, M., Leisinger, T. (1997); Characterization of α-ketoglutarate-dependent taurine dioxygenase from Escherichia coli.. Journal of Biological Chemistry 272:(37)23031–23036 [View Article]
    [Google Scholar]
  16. Foglino, M., Borne, F., Bally, M., Ball, G., Patte, J. C. (1995); A direct sulfhydrylation pathway is used for methionine biosynthesis in Pseudomonas aeruginosa.. Microbiology 141:(2)431–439 [View Article]
    [Google Scholar]
  17. GUnther, E., Petruschka, L., Herrmann, H. (1979); Reverse transsulfuration pathway in Pseudomonas aeruginosa.. Zeitschrift Fur Allgemeine Mikrobiologie 19:439–442
    [Google Scholar]
  18. Hanahan, D. (1983); Transformation of Escherichia coli with plasmids.. ] Mol Biol 166:(4)557–580 [View Article]
    [Google Scholar]
  19. Harvey, N. L., Fewson, C. A., Holms, W. H., Hatt, P. D., Quadroni, M. et al. (1968); Apparatus for batch culture of micro-organisms, Concentration of, and SDS removal from proteins isolated from multiple two dimensional electrophoresis gels.. Lab Pract 246:1134–1136 1968
    [Google Scholar]
  20. Hellinga, H. W., Evans, P. R. (1985); Nucleotide sequence and high-level expression of the major Escherichia coli phospho- fructokinase.. European Journal of Biochemistry 149:(2)363–373 [View Article]
    [Google Scholar]
  21. Hochstrasser, D. F., Harrington, M. G., Hochstrasser, A. C., Miller, M. J., Merril, C. R. (1988); Methods for increasing the resolution of two-dimensional protein electrophoresis.. Analytical Biochemistry 173:(2)424–435 [View Article]
    [Google Scholar]
  22. Hochstrasser, D. F., Frutiger, S., Paquet, N. (1993) & 9 other authors, Human liver reference map: a reference database established by microsequencing and gel comparison.. Electrophoresis 13:(1)992–1001 [View Article]
    [Google Scholar]
  23. Holloway, B. (1955); Genetic recombination in Pseudomonas aeruginosa.. ] Gen Microbiol 13:572–581
    [Google Scholar]
  24. Holloway, B. W., Römling, U., Tümmler B. (1994); Genomic mapping of Pseudomonas aeruginosa PAO.. Microbiology 140:(11)2907–2929 [View Article]
    [Google Scholar]
  25. Jacobson, B. L., Het, J. J., Vermersch, P. S., Lemon, D. D., Quiocho, F. A. (1990); High efficiency transformation of Escherichia coli with plasmids, Engineered interdomain disulfide in the periplasmic receptor for sulfate transport reduces flexibility.. Gene 96:(1)23–28 [View Article]
    [Google Scholar]
  26. Katayama, Y., Hiraishi, A., Kuraishi H. (1995); Paracoccus thiocyanatus sp. nov., a new species of thiocyanate-utilizing facultative chemolithotroph, and transfer of Thiobacillus versutus to the genus Paracoccus as Paracoccus versutus comb, nov. with emendation of the genus.. Microbiology 141:(6)1469–1477 [View Article]
    [Google Scholar]
  27. Kayser, K. J., Bielaga-Jones, B. A., Jackowski, K., Odusan, O., Kilbane J. J. (1993); Utilization of organosulphur compounds by axenic and mixed cultures of Rhodococcus rhodochrous IGTS8.. Journal of General Microbiology 139:(12)3123–3129 [View Article]
    [Google Scholar]
  28. Kennedy, S. I. T., Fewson C. A. (1968); Enzymes of the mandelate pathway in the bacterium NCIB 8250.. Biochemical Journal 107:(4)497–506 [View Article]
    [Google Scholar]
  29. Kertesz, M. A. (1996); Desulfonation of aliphatic sulfonates by Pseudomonas aeruginosa PAO.. Fems Microbiology Letters 137:(2–3)221–225 [View Article]
    [Google Scholar]
  30. Kertesz, M. A., Leisinger, T., Cook A. M. (1993); Proteins induced by sulfate limitation in Escherichia coli, Pseudomonas putida, or Staphylococcus aureus.. Journal of Bacteriology 175:(4)1187–1190 [View Article]
    [Google Scholar]
  31. Kertesz, M. A., Kölbener, P., Stockinger H., Beil S., Cook A. M. (1994); Desulfonation of linear alkylbenzenesulfonate surfactants and related compounds by bacteria.. Appl Environ Microbiol 60:(7)2296–2303 [View Article]
    [Google Scholar]
  32. Kredich, N. M. (1996) Biosynthesis of cysteine.. Edited by Neidhardt, F. C. Escherichia coli and Salmonella. Washington:: American Society for Microbiology,;514–527
    [Google Scholar]
  33. Laudenbach, D. E., Grossman A. (1991); Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: evidence for function in sulfate transport.. Journal of Bacteriology 173:(9)2739–2750 [View Article]
    [Google Scholar]
  34. Leustek, T. (1996); Molecular genetics of sulfate assimilation in plants.. Physiol Plant 97:(2)411–419 [View Article]
    [Google Scholar]
  35. Mazel, D., Marlidre P. (1989); Adaptive eradication of methionine and cysteine from bacterial light-harvesting proteins.. Nature 341:(6239)245–248 [View Article]
    [Google Scholar]
  36. Nagasawa, T., Kanzaki, H., Yamada H. (1987); Cystathionine gamma-lyase from Streptomyces phaeochromogenes.. Methods in Enzymology, Vol 46: Research on Nitrification and Related Processes, Pt B 143:486–493
    [Google Scholar]
  37. O'Hoy, K. (1987); Genetic and physical analysis of the Pseudomonas aeruginosa chromosome,. PhD thesis. Monash University;
  38. Pflugrath, J. W., Quiocho, F. A. (1985); Sulphate sequestered in the sulphate-binding protein of Salmonella typhimurium is bound solely by hydrogen bonds.. Nature 314:(6008)257–260 [View Article]
    [Google Scholar]
  39. van der Ploeg, J. R., Weiss, M. A., Sailer, E., Nashimoto, H., Saito, N. et al. (1996); Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source.. Journal of Bacteriology 178:(18)5438–5446 [View Article]
    [Google Scholar]
  40. Quadroni, M., Staudenmann, W., Kertesz, M., James P. (1996); Analysis of global responses by protein and peptide fingerprinting of proteins isolated by two-dimensional gel electrophoresis.. European Journal of Biochemistry 239:(3)773–781 [View Article]
    [Google Scholar]
  41. Quirk, P. G., Guffanti, A. A., Clejan, S., Cheng, J., Krulwich T. A. (1994); Isolation of Tn917 insertional mutants of Bacillus subtilis that are resistant to the protonophore carbonyl cyanide m- chlorophenylhydrazone.. Biochimica Et Biophysica Acta 1186:(1–2)27–34 [View Article]
    [Google Scholar]
  42. Ratnaningsih, E., Dharmsthiti, S., Krishnapillai, V., Morgan, A., Sinclair, M., Holloway B. W. (1990); A combined physical and genetic map of Pseudomonas aeruginosa PAO.. Journal of General Microbiology 136:(12)2351–2357 [View Article]
    [Google Scholar]
  43. Roberts, R. B., Abelson, P. H., Cowie, D. B.„ Bolton, E., T., Britten, R. J. (1955) Studies of Biosynthesis in Escherichia coli. Washington, DC:: Carnegie Institution;
    [Google Scholar]
  44. Rttmling, U., Duchene, M., Essar, D. W. (1992); 8c 9 other authors, Localization of alg, opr, phn, pho, 4.5S RNA, 6S RNA, tox, trp and xcp genes, rrn operons and the chromosomal origin on the physical genome map of Pseudomonas aeruginosa PAO.. Journal of Bacteriology 174:(1)327–330 [View Article]
    [Google Scholar]
  45. Sanger, F., Nicklen, S., Coulson A. R. (1977); DNA sequencing with chain-terminating inhibitors.. Proc Natl Acad Sci USA 74:(12)5463–5467 [View Article]
    [Google Scholar]
  46. Seitz, A. P., Leadbetter, E. R., Godchaux W., Ill. (1993); Utilization of sulfonates as sole sulfur source by soil bacteria including Comamonas acidovorans.. Archives of Microbiology 159:(5)440–444 [View Article]
    [Google Scholar]
  47. Sirko, A., Zatyka, M., Sadowy, E., Hulanicka D. (1995); Sulfate and thiosulfate transport in Escherichia coli K-12: evidence for a functional overlapping of sulfate- and thiosulfate-binding proteins.. Journal of Bacteriology 177:(14)4134–4136 [View Article]
    [Google Scholar]
  48. Sbrbo, B. (1975) Thiosulfate sulfur transferase and mercapto- pyruvate sulfur transferase.. Edited by Greenberg, D. M. Metabolic Pathways. vol. 7 New York:: Academic Press,;433–456
    [Google Scholar]
  49. Staskawicz, B., Dahlbeck, D., Keen, N., Napoli C. (1987); Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea.. Journal of Bacteriology 169:(12)5789–5794 [View Article]
    [Google Scholar]
  50. Stratford, J., Dias, A. E. X. O., Knowles C. J. (1994); The utilization of thiocyanate as a nitrogen source by a heterotrophic bacterium: the degradative pathway involves formation of ammonia and tetrathionate.. Microbiology 140:(10)2657–2662 [View Article]
    [Google Scholar]
  51. Strickland, T. C., Fitzgerald, J. W., Swank, W. T. (1986); In situmeasurements of sulfate incorporation into forest floor and soil organic matter.. Can J For Res 16:(3)549–553 [View Article]
    [Google Scholar]
  52. Uren, J. R. (1987); Cystathionine beta-lyase from Escherichia coli.. Methods in Enzymology, Vol 46: Research on Nitrification and Related Processes, Pt B 143:483–486
    [Google Scholar]
  53. Uria-Nickelsen, M. R., Leadbetter, E. R., Godchaux, W. Ill (1994); Comparative aspects of utilization of sulfonate and other sulfur sources by Escherichia coli K12.. Archives of Microbiology 161:(5)434–438 [View Article]
    [Google Scholar]
  54. Visca, P., Ciervo, A., Orsi, N. (1994); Cloning and nucleotide sequence of the pvdA gene encoding the pyoverdin biosynthetic enzyme L-ornithine N5-oxygenase in Pseudomonas aeruginosa.. Journal of Bacteriology 176:(4)1128–1140 [View Article]
    [Google Scholar]
  55. Wanner, B. L. (1993); Gene regulation by phosphate in enteric bacteria.. Journal of Cellular Biochemistry 51:(1)47–54 [View Article]
    [Google Scholar]
  56. Watwood, M. E., Fitzgerald, J. W., Gosz, J. R. (1986); Sulfur processing in forest soil and litter along an elevational and vegetative gradient.. Can J For Res 16:(4)689–695 [View Article]
    [Google Scholar]
  57. West, S. E., Iglewski, B. H. (1988); Codon usage in Pseudomonas aeruginosa.. Nucleic Acids Research 16:(19)9323–9325 [View Article]
    [Google Scholar]
  58. Westley, J. (1981); Thiosulfate: cyanide sulfurtransferase (rhodanese).. Methods in Enzymology, Vol 46: Research on Nitrification and Related Processes, Pt B 77:285–291
    [Google Scholar]
  59. ZUrrer, D., Cook, A. M., Leisinger, T. (1987); Microbial desulfonation of substituted naphthalenesulfonic acids and ben- zenesulfonic acids.. Appl Environ Microbiol 53:(7)1459–1463 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-144-5-1375
Loading
/content/journal/micro/10.1099/00221287-144-5-1375
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