1887

Abstract

PAO1 was found to exhibit several remarkable physiological responses to oxidative stress upon its growth in a computer-controlled suspension culture. First, it strongly reduced the transfer rate of oxygen from the gas into the liquid phase, causing oxygen-limited or microaerophilic conditions in the culture after a short period of cultivation, even at high aeration rates with pure oxygen. Second, PAO1 that was previously classified as ’non-mucoid’ formed a clear polysaccharide capsule on the cell surface (mucoid phenotype) under oxidative-stress conditions. Third, the strain showed a reduced growth rate and a longer lag phase under high oxygen tension. Finally, PAO1 released a high amount of proteins into the culture broth. The release of some virulence factors by PAO1, such as elastase, was significantly enhanced or only occurred under microaerobic conditions (i.e. dissolved oxygen tension value around 1% of air saturation). Hence, it is concluded that PAO1 prefers microaerobic conditions for growth and for the formation of some of its virulence factors. PAO1 can create such growth conditions by at least two mechanisms: (i) blockage of the transfer of oxygen and (ii) formation of a polysaccharide capsule on the cell surface. It is postulated that the blockage of oxygen transfer may play an important role in the defence of this pathogen against reactive oxygen intermediates.

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2002-10-01
2024-12-05
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References

  1. Bailey J. E., Ollis D. F. 1985 Biochemical Engineering Fundamentals, 2nd edn. New York: McGraw-Hill;
    [Google Scholar]
  2. Bi J.-X, Wirth M, Beer C, Sabra W., Zeng A.-P. 2001; The use of a C-FOS -GFP reporter system for monitoring apoptosis of animal cells induced by exotoxins of Pseudomonas aeruginosa . In Proceedings of the 17th Meeting of the European Society for Animal Cell Technology, June 10–14 Tylösand, Sweden:
    [Google Scholar]
  3. Bogdan C, Röllinghoff M., Diefenbach A. 2000; Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 12:64–76
    [Google Scholar]
  4. Chayabutra C., Ju L.-K. 2000; Degradation of n-hexadecane and its metabolites by Pseudomonas aeruginosa under microaerobic and anaerobic conditions. Appl Environ Microbiol 66:493–498
    [Google Scholar]
  5. Chayabutra C, Wu J., Ju L.-K. 2001; Rhamnolipid production by Pseudomonas aeruginosa under denitrification: effects of limiting nutrients and carbon substrate. Biotechnol Bioeng 72:25–33
    [Google Scholar]
  6. Costerton J. W, Stewart P. S., Greenberg E. P. 1999; Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1332
    [Google Scholar]
  7. Croft L, Beatson S. A, Whitchurch C. B, Huang B, Blakeley R. L., Mattick J. S. 2000; An interactive web-based Pseudomonas aeruginosa genome database: discovery of new genes, pathways and structures. Microbiology 146:2351–2364
    [Google Scholar]
  8. de Beer D, Stoodley P., Lewandowski Z. 1994; Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol Bioeng 43:1131–1138
    [Google Scholar]
  9. Deretic V, Martin D. W, Schurr M. J, Mudd M. H, Hibler N. S, Curcic R., Boucher J. C. 1993; Conversion to mucoidy in Pseudomonas aeruginosa . Biotechnology 11:1133–1136
    [Google Scholar]
  10. Fyfe J. A. M., Govan J. R. W. 1983; Synthesis, regulation and biological function of bacterial alginate. Prog Ind Microbiol 18:45–83
    [Google Scholar]
  11. Geckil H, Stark B. C., Webster D. A. 2001; Cell growth and growth uptake of Escherichia coli and Pseudomonas aeruginosa are differently affected by the genetically engineered Vitreoscilla hemoglobin gene. J Biotechnol 85:57–66
    [Google Scholar]
  12. Goldberg J. B., Pier G. B. 2000; The role of CFTR in susceptibility to Pseudomonas aeruginosa infections in cystic fibrosis. Trends Microbiol 8:514–520
    [Google Scholar]
  13. Govan J. R. W., Deretic V. 1996; Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia . Microbiol Rev 60:539–574
    [Google Scholar]
  14. Govan J. R. W., Harris G. S. 1986; Pseudomonas aeruginosa and cystic fibrosis: unusual bacterial adaptation and pathogenesis. Microbiol Sci 3:302–308
    [Google Scholar]
  15. Greenberg E. P. 2000; Bacterial genomics. Pump up the versatility. Nature 406:947–948
    [Google Scholar]
  16. Guerra-Santos A, Kaeppeli L. H., Fiechter O. 1986; Dependence of Pseudomonas aeruginosa continuous culture biosurfactant production on nutritional and environmental factors. Appl Microbiol Biotechnol 24:443–448
    [Google Scholar]
  17. Haba E, Espuny M. J, Busquets M., Manresa A. 2000; Screening and production of rhamnolipids by Pseudomonas aeruginosa 47T2 NCIB 40044 from waste frying oils. J Appl Microbiol 88:379–387
    [Google Scholar]
  18. Ishida H, Ishida Y, Kurosaka Y, Otani T, Sato K., Kobayashi H. 1998; In vitro and in vivo activities of levofloxacin against biofilm-producing Pseudomonas aeruginosa . Antimicrob Agents Chemother 42:1641–1645
    [Google Scholar]
  19. Kamath S, Kapatral V., Chakrabarty A. M. 1998; Cellular function of elastase in Pseudomonas aeruginosa : role in the cleavage of nucleoside diphosphate kinase and in alginate synthesis. Mol Microbiol 30:933–941
    [Google Scholar]
  20. Kessler E, Safrin M, Olson J. C., Ohman D. E. 1993; Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem 268:7503–7508
    [Google Scholar]
  21. Kharazmi A. 1991; Mechanisms involved in the evasion of the host defence by Pseudomonas aeruginosa . Immunol Lett 30201–205
    [Google Scholar]
  22. Knutson C. A., Jeanes A. 1968; Determination of the composition of uronic acid mixtures. Anal Biochem 24:482–490
    [Google Scholar]
  23. Kock A. K, Käppeli O, Fiechter A., Reiser J. 1991; Hydrocarbon assimilation and biosurfactant production in Pseudomonas aeruginosa mutants. J Bacteriol 173:4212–4219
    [Google Scholar]
  24. Krieg D. P, Bass J. A., Mattingly S. J. 1986; Aeration selects for mucoid phenotype of Pseudomonas aeruginosa . J Clin Microbiol 24:986–990
    [Google Scholar]
  25. Leitäo J. H., Sä-Correia I. 1997; Oxygen-dependent upregulation of transcription of alginate genes algA , algC and algD in Pseudomonas aeruginosa . Res Microbiol 148:37–43
    [Google Scholar]
  26. Maier R. M., Soberon-Chavez G. 2000; Pseudomonas aeruginosa rhamnolipids: biosynthesis and potential applications. Appl Microbiol Biotechnol 54:625–633
    [Google Scholar]
  27. Mathee K, Ciofu O, Sternberg C. 9 other authors 1999; Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 145:1349–1357
    [Google Scholar]
  28. Mian F. A, Jarman T. R., Righelato R. C. 1978; Biosynthesis of exopolysaccharide by Pseudomonas aeruginosa . J Bacteriol 134:418–422
    [Google Scholar]
  29. Miller R. A., Britigan B. E. 1997; Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 10:1–18
    [Google Scholar]
  30. Nathan C., Shiloh M. U. 2000; Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA 97:8841–8848
    [Google Scholar]
  31. Pearson J. P, Pesci E. C., Iglewski B. H. 1997; Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179:5756–5767
    [Google Scholar]
  32. Pier G. B. 1998; Pseudomonas aeruginosa : a key problem in cystic fibrosis. ASM News 64:339–347
    [Google Scholar]
  33. Rocha C, San-Blas F, San-Blas G., Vierma L. 1992; Biosurfactant production by two isolates of Pseudomonas aeruginosa . World J Microbiol Biotechnol 8:125–128
    [Google Scholar]
  34. Rumbaugh K. P, Griswold J. A, Iglewski B. H., Hamood A. N. 1999; Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect Immun 67:5854–5862
    [Google Scholar]
  35. Sabra W, Zeng A.-P, Sabry S, Omar S., Deckwer W.-D. 1999; Effect of phosphate and oxygen concentrations on alginate production and stoichiometry of metabolism of Azotobacter vinelandii under microaerobic conditions. Appl Microbiol Biotechnol 52:773–780
    [Google Scholar]
  36. Sabra W, Zeng A.-P, Lünsdorf H., Deckwer W.-D. 2000; Effect of oxygen on formation and structure of Azotobacter vinelandii alginate and its role in protecting nitrogenase. Appl Environ Microbiol 66:4037–4044
    [Google Scholar]
  37. Sabra W, Zeng A.-P., Deckwer W.-D. 2001; Bacterial alginate: physiology, product quality and process aspects. Appl Microbiol Biotechnol 56:315–325
    [Google Scholar]
  38. Sato S, Mukataka S, Kataoka H., Takahashi J. 1984; Effects of pressure and dissolved oxygen concentration on growth of Pseudomonas aeruginosa . J Ferment Technol 62:71–75
    [Google Scholar]
  39. Shellito J, Nelson S., Sorensen R. U. 1992; Effect of pyocyanine, a pigment of Pseudomonas aeruginosa , on production of reactive nitrogen intermediates by murine alveolar macrophages. Infect Immun 60:3913–3915
    [Google Scholar]
  40. Stanbury P. F., Whitaker A. 1987 Principles of Fermentation Technology Edited by Stanbury P. F., Whitaker A. Oxford: Pergamon;
    [Google Scholar]
  41. Xu K. D, Stewart P. S, Xia F, Huang C.-T., McFeters G. A. 1998; Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl Environ Microbiol 64:4035–4039
    [Google Scholar]
  42. Zaborina O, Dhiman N, Ling Chen M, Kostal J, Holder I. A., Chakrabarty A. M. 2000; Secreted products of a nonmucoid Pseudomonas aeruginosa strain induce two modes of macrophage killing: external-ATP-dependent, PZZ-receptor-mediated necrosis and ATP-independent, caspase-mediated apoptosis. Microbiology 146:2521–2530
    [Google Scholar]
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