1887

Abstract

PAO1 was recently found to exhibit two remarkable physiological responses to oxidative stress: (1) a strong reduction in the efficiency of oxygen transfer from the gas phase into the liquid phase, thus causing oxygen limitation in the culture and (2) formation of a clear polysaccharide capsule on the cell surface. In this work, it has been shown that the iron concentration in the culture plays a crucial role in evoking these phenomena. The physiological responses of two PAO1 isolates (NCCB 2452 and ATCC 15692) were examined in growth media with varied iron concentrations. In a computer-controlled bioreactor cultivation system for controlled dissolved oxygen tension (O), a strong correlation between the exhaustion of iron and the onset of oxygen limitation was observed. The oxygen transfer rate of the culture, characterized by the volumetric oxygen transfer coefficient, , significantly decreased under iron-limited conditions. The formation of alginate and capsule was more strongly affected by iron concentration than by oxygen concentration. The reduction of the oxygen transfer rate and the subsequent oxygen limitation triggered by iron deficiency may represent a new and efficient way for PAO1 to adapt to growth conditions of iron limitation. Furthermore, the secretion of proteins into the culture medium was strongly enhanced by iron limitation. The formation of the virulence factor elastase and the iron chelators pyoverdine and pyochelin also significantly increased under iron-limited conditions. These results have implications for lung infection of cystic fibrosis patients by in view of the prevalence of iron limitation at the site of infection and the respiratory failure leading to death.

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2003-09-01
2019-11-17
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References

  1. Andrews, S. C. ( 1998; ). Iron storage in bacteria. Adv Microb Physiol 40, 281–351.
    [Google Scholar]
  2. Ankenbauer, R., Sriyosachati, S. & Cox, C. D. ( 1985; ). Effects of siderophores on the growth of Pseudomonas aeruginosa in human serum and transferrin. Infect Immun 49, 132–140.
    [Google Scholar]
  3. Bjorn, M. J., Sokol, P. A. & Iglewski, B. H. ( 1979; ). Influence of iron on yields of extracellular products in Pseudomonas aeruginosa cultures. J Bacteriol 138, 193–200.
    [Google Scholar]
  4. Britigan, B. E., Rasmussen, G. T. & Cox, C. D. ( 1998; ). Binding of iron and inhibition of iron dependent oxidative cell injury by the ‘Calcium chelator’ 1,2-bis(2-aminophenoxy)ethane N,N,N′,N′-tetraacetic acid (BAPTA). Biochem Pharmacol 55, 287–295.[CrossRef]
    [Google Scholar]
  5. Brumlik, M. J. & Storey, D. G. ( 1992; ). Zinc and iron regulate translation of the gene encoding Pseudomonas aeruginosa elastase. Mol Microbiol 6, 337–344.[CrossRef]
    [Google Scholar]
  6. Chayabutra, C. & Ju, L. K. ( 2000; ). Degradation of n-hexadecane and its metabolites by Pseudomonas aeruginosa under microaerobic and anaerobic denitrifying conditions. Appl Environ Microbiol 66, 493–498.[CrossRef]
    [Google Scholar]
  7. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. ( 1999; ). Bacterial biofilms: a common cause of persistent infections. Science 284, 1318–1332.[CrossRef]
    [Google Scholar]
  8. Cowart, R. E. ( 2002; ). Reduction of iron by extracellular iron reductases: implications for microbial iron acquisition. Arch Biochem Biophys 400, 273–281.[CrossRef]
    [Google Scholar]
  9. Cox, C. D. ( 1982; ). Effect of pyochelin on the virulence of Pseudomonas aeruginosa. Infect Immun 36, 17–23.
    [Google Scholar]
  10. Cox, C. D. ( 1986; ). Role of pyocyanin in the acquisition of iron from transferrin. Infect Immun 52, 263–270.
    [Google Scholar]
  11. Elkins, J. G., Hassett, D. J., Stewart, P. S., Schweizer, H. P. & McDermott, T. R. ( 1999; ). Protective role of catalase in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide. Appl Environ Microbiol 65, 4595–4600.
    [Google Scholar]
  12. Forsberg, C. M. & Bullen, J. J. ( 1972; ). The effect of passage and iron on the virulence of Pseudomonas aeruginosa. J Clin Pathol 25, 65–68.
    [Google Scholar]
  13. Frederick, J. R., Elkins, J. G., Bollinger, N., Hassett, D. J. & McDermott, T. R. ( 2001; ). Factors affecting catalase expression in Pseudomonas aeruginosa biofilms and planktonic cells. Appl Environ Microbiol 67, 1375–1379.[CrossRef]
    [Google Scholar]
  14. Geckil, H., Stark, B. C. & Webster, D. A. ( 2001; ). Cell growth and oxygen uptake of Escherichia coli and Pseudomonas aeruginosa are differently effected by the genetically engineered Vitreoscilla hemoglobin gene. J Biotechnol 85, 57–66.[CrossRef]
    [Google Scholar]
  15. 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]
  16. Griffiths, E., Chart, H. & Stevenson, P. ( 1988; ). High affinity iron uptake systems and bacterial virulence. In Virulence Mechanisms of Bacterial Pathogens, pp. 121–137. Edited by J. A. Roth. Washington, DC: American Society for Microbiology.
  17. Hassett, D. J., Ma, J. F., Elkins, J. G. & 10 other authors ( 1999; ). Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 34, 1082–1093.[CrossRef]
    [Google Scholar]
  18. Kessler, E., Safrin, M., Olsan, J. C. & Ohman, D. E. ( 1993; ). Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem 268, 7503–7508.
    [Google Scholar]
  19. 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.[CrossRef]
    [Google Scholar]
  20. McMorran, B. J., Kumara, H. M. C. S., Sullivan, K. & Lamont, I. L. ( 2001; ). Involvement of a transformylase enzyme in siderophore synthesis in Pseudomonas aeruginosa. Microbiology 147, 1517–1524.
    [Google Scholar]
  21. Mian, F. A., Jarman, T. R. & Righelato, R. C. ( 1978; ). Biosynthesis of exopolysaccharide by Pseudomonas aeruginosa. J Bacteriol 134, 418–422.
    [Google Scholar]
  22. Miller, R. A. & Britigan, B. E. ( 1997; ). Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 10, 1–18.
    [Google Scholar]
  23. Ratledge, C. & Dover, L. G. ( 2000; ). Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54, 881–941.[CrossRef]
    [Google Scholar]
  24. 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.[CrossRef]
    [Google Scholar]
  25. Sabra, W., Kim, E.-J. & Zeng, A.-P. ( 2002; ). Physiological responses of Pseudomonas aeruginosa PAO1 to oxidative stress in controlled microaerobic and aerobic cultures. Microbiology 148, 3195–3202.
    [Google Scholar]
  26. Schalk, I. J., Abdallah, M. A. & Pattus, F. ( 2002; ). A new mechanism for membrane iron transport in Pseudomonas aeruginosa. Biochem Soc Trans 30, 702–705.
    [Google Scholar]
  27. Stanbury, P. F. & Whitaker, A. (editors) ( 1987; ). Principles of Fermentation Technology. Oxford: Pergamon Press.
  28. Stewart, P. S., Roe, F., Rayner, J., Elkins, J. G., Lewandowski, Z., Ochsner, U. A. & Hassett, D. J. ( 2000; ). Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 66, 836–838.[CrossRef]
    [Google Scholar]
  29. Stintzi, A., Evans, K., Meyer, J. M. & Poole, K. ( 1998; ). Quorum sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol Lett 166, 341–345.[CrossRef]
    [Google Scholar]
  30. Storey, D. G., Ujack, E. E. & Rabin, H. R. ( 1992; ). Population transcript accumulation of Pseudomonas aeruginosa exotoxin A and elastase in sputa from patients with cystic fibrosis. Infect Immun 60, 4687–4694.
    [Google Scholar]
  31. Valente, E., Assis, M. C., Alvim, I. M. P., Pereira, G. M. B. & Plotkowski, M. C. ( 2000; ). Pseudomonas aeruginosa induces apoptosis in human endothelial cells. Microb Pathog 29, 345–358.[CrossRef]
    [Google Scholar]
  32. Vasil, M. L. & Ochsner, U. A. ( 1999; ). The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol Microbiol 34, 399–413.[CrossRef]
    [Google Scholar]
  33. Wolz, C., Hohloch, K., Ocaktan, A., Poole, K., Evans, R. W., Rochel, N., Albrecht-Gary, A. M., Abdallah, M. A. & Döring, G. ( 1994; ). Iron release from transferrin by pyoverdine and elastase from Pseudomonas aeruginosa. Infect Immun 62, 4021–4027.
    [Google Scholar]
  34. 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]
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