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
2019-10-13
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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  4. Blumer, C. & Haas, D. ( 2000; ). Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Arch Microbiol 173, 170–177.[CrossRef]
    [Google Scholar]
  5. Castric, P. A. ( 1975; ). Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Can J Microbiol 21, 613–618.[CrossRef]
    [Google Scholar]
  6. Castric, P. A. ( 1983; ). Hydrogen cyanide production by Pseudomonas aeruginosa at reduced oxygen levels. Can J Microbiol 29, 1344–1349.[CrossRef]
    [Google Scholar]
  7. Castric, P. ( 1994; ). Influence of oxygen on the Pseudomonas aeruginosa hydrogen-cyanide synthase. Curr Microbiol 29, 19–21.[CrossRef]
    [Google Scholar]
  8. Castric, P., Ebert, R. F. & Castric, K. F. ( 1979; ). The relationship between growth phase and cyanogenesis. Curr Microbiol 2, 287–292.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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 J. P. Natarro, M. J. Blaser & S. Cunningham-Rundles. Washington, DC: American Society for Microbiology.
  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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  22. Goldfarb, W. B. & Margraf, H. ( 1967; ). Cyanide production by Pseudomonas aeruginosa. Ann Surg 165, 104–110.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  27. Iuchi, S. & Lin, E. C. ( 1993; ). Adaptation of Escherichia coli to redox environments by gene expression. Mol Microbiol 9, 9–15.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  29. Junemann, S. ( 1997; ). Cytochrome bd terminal oxidase. Biochim Biophys Acta 1321, 107–127.[CrossRef]
    [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.[CrossRef]
    [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.
  34. Oh, J. I. & Kaplan, S. ( 2000; ). Redox signaling: globalization of gene expression. EMBO J 19, 4237–4247.[CrossRef]
    [Google Scholar]
  35. Oh, J. I. & Kaplan, S. ( 2001; ). Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39, 1116–1123.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  37. Palleroni, N. J. ( 1984; ). Family I. Pseudomonadaceae. In Bergey's Manual of Systematic Bacteriology, vol. 1, pp. 141–219. Edited by N. R. Krieg & J. G. Holt. Baltimore: Williams & Wilkins.
  38. Pirt, S. J. ( 1975; ). Oxygen demand and supply. In Principles of Microbe and Cell Cultivation, pp. 81–116. Oxford: Blackwell.
  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.[CrossRef]
    [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.[CrossRef]
    [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.
  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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  58. Zannoni, D. ( 1989; ). The respiratory chains of pathogenic pseudomonads. Biochim Biophys Acta 975, 299–316.[CrossRef]
    [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.[CrossRef]
    [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