1887

Abstract

The regulation of the cyanide-insensitive oxidase (CIO) in , a bacterium that can synthesize HCN, is reported. The expression of a transcriptional fusion, CioA protein levels and CIO activity were low in exponential phase but induced about fivefold upon entry into stationary phase. Varying the O transfer coefficient from 11·5 h to 87·4 h had no effect on CIO expression and no correlation was observed between CIO induction and the dissolved O levels in the growth medium. However, a mutant deleted for the O-sensitive transcriptional regulator ANR derepressed CIO expression in an O-sensitive manner, with the highest induction occurring under low-O conditions. Therefore, CIO expression can respond to a signal generated by low O levels, but this response is normally kept in check by ANR repression. ANR may play an important role in preventing overexpression of the CIO in relation to other terminal oxidases. A component present in spent culture medium was able to induce CIO expression. However, experiments with purified -butanoyl--homoserine lactone or -(3-oxododecanoyl)homoserine lactone ruled out a role for these quorum-sensing molecules in the control of CIO expression. Cyanide was a potent inducer of the CIO at physiologically relevant concentrations and experiments using spent culture medium from a Δ mutant, which is unable to synthesize cyanide, showed that cyanide was the inducing factor present in spent culture medium. However, the finding that in a Δ mutant expression was induced normally upon entry into stationary phase indicated that cyanide was not the endogenous inducer of the terminal oxidase. The authors suggest that the failure of O to have an effect on CIO expression in the wild-type can be explained either by the requirement for an additional, stationary-phase-specific inducing signal or by the loss of an exponential-phase-specific repressing signal.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26017-0
2003-05-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/5/mic1491275.html?itemId=/content/journal/micro/10.1099/mic.0.26017-0&mimeType=html&fmt=ahah

References

  1. Arai H., Igarashi Y., Kodama T. 1994; Structure and Anr-dependent transcription of the nir genes for denitrification from Pseudomonas aeruginosa . Biosci Biotechnol Biochem 58:1286–1291
    [Google Scholar]
  2. Arai H., Igarashi Y., Kodama T. 1995; Expression of the nir and nor genes for denitrification of Pseudomonas aeruginosa requires a novel Crp/Fnr-related transcriptional regulator, Dnr, in addition to Anr. FEBS Lett 371:73–76
    [Google Scholar]
  3. Arai H., Kodama T., Igarashi Y. 1997; Cascade regulation of the two Crp/Fnr-related transcriptional regulators (Anr and Dnr) and the denitrification enzymes in Pseudomonas aeruginosa . Mol Microbiol 25:1141–1148
    [Google Scholar]
  4. Blumer C., Haas D. 2000; Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Arch Microbiol 173:170–177
    [Google Scholar]
  5. Castric P. A. 1975; Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa . Can J Microbiol 21:613–618
    [Google Scholar]
  6. Castric P. A. 1983; Hydrogen cyanide production by Pseudomonas aeruginosa at reduced oxygen levels. Can J Microbiol 29:1344–1349
    [Google Scholar]
  7. Castric P. 1994; Influence of oxygen on the Pseudomonas aeruginosa hydrogen-cyanide synthase. Curr Microbiol 29:19–21
    [Google Scholar]
  8. Castric P., Ebert R. F., Castric K. F. 1979; The relationship between growth phase and cyanogenesis. Curr Microbiol 2:287–292
    [Google Scholar]
  9. Comolli J. C., Donohue T. J. 2002; Pseudomonas aeruginosa RoxR, a response regulator related to Rhodobacter sphaeroides PrrA, activates expression of the cyanide-insensitive terminal oxidase. Mol Microbiol 45:755–768
    [Google Scholar]
  10. Cunningham L., Williams H. D. 1995; Isolation and characterization of mutants defective in the cyanide-insensitive respiratory pathway of Pseudomonas aeruginosa . J Bacteriol 177:432–438
    [Google Scholar]
  11. Cunningham L., Pitt M., Williams H. D. 1997; The cioAB genes from Pseudomonas aeruginosa code for a novel cyanide-insensitive terminal oxidase related to the cytochrome bd quinol oxidases. Mol Microbiol 24:579–591
    [Google Scholar]
  12. Davies K. J., Lloyd D., Boddy L. 1989; The effect of oxygen on denitrification in Paracoccus denitrificans and Pseudomonas aeruginosa . J Gen Microbiol 135:2445–2451
    [Google Scholar]
  13. Deretic V. 2000; Pseudomonas aeruginosa . In Persistent Bacterial Infections pp  305–326 Edited by Natarro J. P., Blaser M. J., Cunningham-Rundles S. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  14. D'Mello R., Hill S., Poole R. K. 1994; Determination of the oxygen affinities of the terminal oxidases in Azotobacter vinelandii using the deoxygenation of oxyleghaemoglobin and oxymyoglobin – cytochrome bd is a low-affinity oxidase. Microbiology 140:1395–1402
    [Google Scholar]
  15. Dueweke T. J., Gennis R. B. 1990; Epitopes of monoclonal-antibodies which inhibit ubiquinol oxidase activity of Escherichia coli cytochrome- d complex localize functional domain. J Biol Chem 265:4273–4277
    [Google Scholar]
  16. Fuqua C., Greenberg E. P. 1998; Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr Opin Microbiol 1:183–189
    [Google Scholar]
  17. Galimand M., Gamper M., Zimmermann A., Haas D. 1991; Positive FNR-like control of anaerobic arginine degradation and nitrate respiration in Pseudomonas aeruginosa . J Bacteriol 173:1598–1606
    [Google Scholar]
  18. Gallagher L. A., Manoil C. 2001; Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J Bacteriol 183:6207–6214
    [Google Scholar]
  19. Garcia-Horsman J. A., Barquera B., Rumbley J., Ma J., Gennis R. B. 1994; The superfamily of heme-copper respiratory oxidases. J Bacteriol 176:5587–5600
    [Google Scholar]
  20. Georgellis D., Kwon O., Lin E. C. 2001; Quinones as the redox signal for the arc two-component system of bacteria. Science 292:2314–2316
    [Google Scholar]
  21. Gil A., Kroll R. G., Poole R. K. 1992; The cytochrome composition of the meat spoilage bacterium Brochothrix thermosphacta ; identification of cytochrome a 3- and d -type terminal oxidases under various conditions. Arch Microbiol 158:226–233
    [Google Scholar]
  22. Goldfarb W. B., Margraf H. 1967; Cyanide production by Pseudomonas aeruginosa . Ann Surg 165:104–110
    [Google Scholar]
  23. Govan J. R., Deretic V. 1996; Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia . Microbiol Rev 60:539–574
    [Google Scholar]
  24. Hasegawa N., Arai H., Igarashi Y. 1998; Activation of a consensus Fnr-dependent promoter by Dnr of Pseudomonas aeruginosa in response to nitrite. FEMS Microbiol Lett 166:213–217
    [Google Scholar]
  25. Hassett D. J. 1996; Anaerobic production of alginate by Pseudomonas aeruginosa : alginate restricts diffusion of oxygen. J Bacteriol 178:7322–7325
    [Google Scholar]
  26. Holloway B. W., Romling U., Tummler B. 1994; Genomic mapping of Pseudomonas aeruginosa PAO. Microbiology 140:2907–2929
    [Google Scholar]
  27. Iuchi S., Lin E. C. 1993; Adaptation of Escherichia coli to redox environments by gene expression. Mol Microbiol 9:9–15
    [Google Scholar]
  28. Jorgensen F., Bally M., Chaponherve V., Michel G., Lazdunski A., Williams P., Stewart G. S. A. B. 1999; RpoS-dependent stress tolerance in Pseudomonas aeruginosa . Microbiology 145:835–844
    [Google Scholar]
  29. Junemann S. 1997; Cytochrome bd terminal oxidase. Biochim Biophys Acta 1321107–127
    [Google Scholar]
  30. Latifi A., Foglino M., Tanaka K., Williams P., Lazdunski A. A. 1996; Hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhiR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21:1137–1146
    [Google Scholar]
  31. Matsushita K., Yamada M., Shinagawa E., Adachi O., Ameyama M. 1980; Membrane-bound respiratory chain of Pseudomonas aeruginosa grown aerobically. J Bacteriol 141:389–392
    [Google Scholar]
  32. Matsushita K., Yamada M., Shinagawa E., Adachi O., Ameyama M. 1983; Membrane-bound respiratory chain of Pseudomonas aeruginosa grown aerobically. A KCN-insensitive alternate oxidase chain and its energetics. J Biochem 93:1137–1144
    [Google Scholar]
  33. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  34. Oh J. I., Kaplan S. 2000; Redox signaling: globalization of gene expression. EMBO J 19:4237–4247
    [Google Scholar]
  35. Oh J. I., Kaplan S. 2001; Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39:1116–1123
    [Google Scholar]
  36. Otten M. F., Stork D. M., Reijnders W. N., Westerhoff H. V., Van Spanning R. J. 2001; Regulation of expression of terminal oxidases in Paracoccus denitrificans . Eur J Biochem 268:2486–2497
    [Google Scholar]
  37. Palleroni N. J. 1984; Family I. Pseudomonadaceae .In Bergey's Manual of Systematic Bacteriology vol. 1 pp  141–219 Edited by Krieg N. R., Holt J. G. Baltimore: Williams & Wilkins;
    [Google Scholar]
  38. Pirt S. J. 1975; Oxygen demand and supply. In Principles of Microbe and Cell Cultivation pp  81–116 Oxford: Blackwell;
    [Google Scholar]
  39. Poole R. K., Cook G. M. 2000; Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation. Adv Microb Physiol 43:165–224
    [Google Scholar]
  40. Ray A., Williams H. D. 1996; A mutant of Pseudomonas aeruginosa that lacks c -type cytochromes has a functional cyanide-insensitive oxidase. FEMS Microbiol Lett 135:123–129
    [Google Scholar]
  41. Ray A., Williams H. D. 1997; The effects of mutation of the anr gene on the aerobic respiratory chain of Pseudomonas aeruginosa . FEMS Microbiol Lett 156:227–232
    [Google Scholar]
  42. Richardson D. J. 2000; Bacterial respiration: a flexible process for a changing environment. Microbiology 146:551–571
    [Google Scholar]
  43. Rothmel R. K., Chakrabarty A. M., Berry A., Darzins A. 1991; Genetic systems in Pseudomonas . Methods Enzymol 204:485–514
    [Google Scholar]
  44. Ruchti G., Dunn I. J., Bourne J. R., Vonstockar U. 1985; Practical guidelines for the determination of oxygen-transfer coefficients ( k L a ) with the sulfite oxidation method. Chem Eng J Biochem Eng J 30:29–38
    [Google Scholar]
  45. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  46. Sawers R. G. 1991; Identification and molecular characterization of a transcriptional regulator from Pseudomonas aeruginosa PAO1 exhibiting structural and functional similarity to the FNR protein of Escherichia coli . Mol Microbiol 5:1469–1481
    [Google Scholar]
  47. Spaink H. P., Okker R. J. H., Wijffelman C. A., Pees E., Lugtenberg B. J. J. 1987; Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol Biol 9:27–39
    [Google Scholar]
  48. Stover C. K., Pham X. Q., Erwin A. L. 28 other authors 2000; Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959–964
    [Google Scholar]
  49. Suh S. J., Silosuh L., Woods D. E., Hassett D. J., West S. E. H., Ohman D. E. 1999; Effect of rpoS mutation on the stress response and expression of virulence factors in Pseudomonas aeruginosa . J Bacteriol 181:3890–3897
    [Google Scholar]
  50. Swift S., Downie J. A., Whitehead N. A., Barnard A. M., Salmond G. P., Williams P. 2001; Quorum sensing as a population-density-dependent determinant of bacterial physiology. Adv Microb Physiol 45:199–270
    [Google Scholar]
  51. Tanaka K., Takahashi H. 1994; Cloning, analysis and expression of an rpoS homolog gene from Pseudomonas aeruginosa PAO1. Gene 150:81–85
    [Google Scholar]
  52. Tavankar G. R., Mossialos D., Williams H. D. 2003; Mutation or overexpression of a terminal oxidase leads to a cell division defect and multiple antibiotic sensitivity in Pseudomonas aeruginosa . J Biol Chem 278:4524–4530
    [Google Scholar]
  53. Van der Wauven C., Pierard A., Kleyraymann M., Haas D. 1984; Pseudomonas aeruginosa mutants affected in anaerobic growth on arginine – evidence for a 4-gene cluster encoding the arginine deiminase pathway. J Bacteriol 160:928–934
    [Google Scholar]
  54. Withers H., Swift S., Williams P. 2001; Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr Opin Microbiol 4:186–193
    [Google Scholar]
  55. Worlitzsch D., Tarran R., Ulrich M. 12 other authors 2002; Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109:317–325
    [Google Scholar]
  56. Ye R. W., Haas D., Ka J. O., Krishnapillai V., Zimmermann A., Baird C., Tiedje J. M. 1995; Anaerobic activation of the entire denitrification pathway in Pseudomonas aeruginosa requires Anr, an analog of Fnr. J Bacteriol 177:3606–3609
    [Google Scholar]
  57. You Z., Fukushima J., Tanaka K., Kawamoto S., Okuda K. 1998; Induction of entry into the stationary growth phase in Pseudomonas aeruginosa by N -acylhomoserine lactone. FEMS Microbiol Lett 164:99–106
    [Google Scholar]
  58. Zannoni D. 1989; The respiratory chains of pathogenic pseudomonads. Biochim Biophys Acta 975:299–316
    [Google Scholar]
  59. Zimmermann A., Reimmann C., Galimand M., Haas D. 1991; Anaerobic growth and cyanide synthesis of Pseudomonas aeruginosa depend on anr , a regulatory gene homologous with fnr of Escherichia coli . Mol Microbiol 5:1483–1490
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26017-0
Loading
/content/journal/micro/10.1099/mic.0.26017-0
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