1887

Abstract

The haem pigment of is composed of -oxo bishaem, [Fe(III)PPIX]O, but the nature of that generated by species has not been established. Mössbauer, Raman and UV-visible spectrophotometry were used to characterize the haem pigment of and . Mössbauer and Raman spectroscopy revealed the major haem species to be monomeric iron protoporphyrin IX, Fe(III)PPIX.OH (haematin). The terminal growth pH of both species on blood agar was between 5·8 and 6·0, which favours the formation and maintenance of monomeric Fe(III)PPIX.OH. Incubation of and with oxyhaemoglobin at pH 6·5 resulted in formation of aquomethaemoglobin which was degraded to generate Fe(III)PPIX.OH which in turn became cell-associated, whilst incubation at pH 7·5 resulted in formation of [Fe(III)PPIX]O. It is concluded that both species degrade oxyhaemoglobin to form [Fe(III)PPIX]O as an intermediate, which is converted to Fe(III)PPIX.OH through a depression in pH. The low pH encourages cell-surface deposition of insoluble Fe(III)PPIX.OH which would act as a barrier against oxygen and reactive oxygen species, and also protect against HO through its inherent catalase activity.

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2003-07-01
2019-11-15
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References

  1. Antonini, E. & Brunori, M. ( 1971; ). The derivatives of ferric hemoglobin and myoglobin. In Hemoglobin and Myoglobin and Their Reactions with Ligands. North Holland Research Monographs Frontiers of Biology, vol. 21, pp. 40–54. Edited by A. Neuberger & E. L. Tatum. Amsterdam: North Holland Publishing Company.
  2. Bickel, M. & Cimasoni, G. ( 1985; ). The pH of human crevicular fluid measured by a new microanalytical technique. J Periodont Res 20, 35–40.[CrossRef]
    [Google Scholar]
  3. Carlsson, J., Hofling, J. F. & Sundqvist, G. K. ( 1984; ). Degradation of albumin, haemopexin, haptoglobin and transferrin, by black-pigmented Bacteroides species. J Med Microbiol 18, 39–46.[CrossRef]
    [Google Scholar]
  4. Cornelius, V. J., Titler, P. J., Fern, G. R., Miller, J. R., Silver, J. & McCammon, C. A. ( 2003; ). An interesting spin state transition for [Fe(PPIX)OH] induced by the application of high pressure in a diamond anvil cell. Hyperfine Interact 144 (in press).
    [Google Scholar]
  5. Finegold, S. M., Strong, C. A., McTeague, M. & Marina, M. ( 1993; ). The importance of black-pigmented gram-negative anaerobes in human infections. FEMS Immunol Med Microbiol 6, 77–82.[CrossRef]
    [Google Scholar]
  6. Garcia-Mendoza, A., Liebana, J., Castillo, A. M., de la Higuera, A. & Piedrola, G. ( 1993; ). Evaluation of the capacity of oral streptococci to produce hydrogen peroxide. J Med Microbiol 39, 434–439.[CrossRef]
    [Google Scholar]
  7. Guan, S., Nagata, H., Kubiniwa, M., Ikawa, Y., Maeda, K. & Shizukuishi, S. ( 2002; ). Characterization of binding and utilization of hemoglobin by Prevotella nigrescens. Oral Microbiol Immunol 17, 157–162.[CrossRef]
    [Google Scholar]
  8. Hameed, M. Y., Hider, R. C. & Silver, J. ( 1982; ). The competition between enterobactin and glutathione for iron. Inorg Chim Acta 66, 13–18.[CrossRef]
    [Google Scholar]
  9. Hirst, I. D., Hastings, T. S. & Ellis, A. E. ( 1994; ). Utilisation of heme compounds by Aeromonas salmonicida. J Fish Dis 17, 365–373.[CrossRef]
    [Google Scholar]
  10. Jansen, H.-J., van der Hoeven, J. S., Göertz, J. H. C. & Bakkeren, J. A. J. M. ( 1994; ). Breakdown of various serum components by periodontal bacteria. Microb Ecol Health D 7, 299–305.[CrossRef]
    [Google Scholar]
  11. Jones, P., Robson, T. & Brown, S. B. ( 1973; ). The catalase activity of ferrihaems. Biochem J 135, 353–359.
    [Google Scholar]
  12. Keilin, D. & Hartree, E. F. ( 1951; ). Purification of horse-radish peroxidase and comparison of its properties with those of catalase and methaemoglobin. Biochem J 49, 88–104.
    [Google Scholar]
  13. Kohlenbrander, P. E. ( 1988; ). Intergeneric coaggregation among human oral bacteria and ecology of dental plaque. Annu Rev Microbiol 42, 627–656.[CrossRef]
    [Google Scholar]
  14. Leung, K. P., Subramaniam, P. S., Okamoto, M., Fukushima, H. & Lai, C. H. ( 1998; ). The binding and utilization of hemoglobin by Prevotella intermedia. FEMS Microbiol Lett 162, 227–233.[CrossRef]
    [Google Scholar]
  15. McDermid, A. S., McKee, A. S. & Marsh, P. D. ( 1988; ). Effect of environmental pH on enzyme activity and growth of Bacteroides gingivalis W50. Infect Immun 56, 1096–1100.
    [Google Scholar]
  16. Mettraux, G. R., Gusberti, F. A. & Graf, H. ( 1984; ). Oxygen tension (pO2) in untreated human periodontal pockets. J Periodontol 55, 516–521.[CrossRef]
    [Google Scholar]
  17. Moore, L. V. H., Moore, W. E. C., Cato, E. P., Smibert, R. M., Burmeister, J. A., Best, A. M. & Ranney, R. R. ( 1987; ). Bacteriology of human gingivitis. J Dent Res 66, 989–995.[CrossRef]
    [Google Scholar]
  18. Moore, W. E. C., Holdeman, L. V., Cato, E. P., Smibert, R. M., Burmeister, J. A. & Ranney, R. R. ( 1983; ). Bacteriology of moderate (chronic) periodontitis in humans. Infect Immun 42, 510–515.
    [Google Scholar]
  19. Pendrak, M. L. & Perry, R. D. ( 1997; ). Proteins essential for expression of the Hms+ phenotype of Yersinia pestis. Mol Microbiol 8, 857–864.
    [Google Scholar]
  20. Rawlinson, A., Duerden, B. I. & Goodwin, L. ( 1991; ). Microbial flora of bleeding and non-bleeding pockets of variable depth in adult periodontitis. Microb Ecol Health D 4, 383–389.[CrossRef]
    [Google Scholar]
  21. Rawlinson, A., Duerden, B. I. & Goodwin, L. ( 1993; ). New findings on the microbial flora associated with adult periodontitis. J Dent Res 21, 179–184.[CrossRef]
    [Google Scholar]
  22. Rizza, V., Sinclair, P. R., White, D. C. & Courant, P. R. ( 1968; ). Electron transport system of the protoheme-requiring anaerobe Bacteroides melaninogenicus. J Bacteriol 96, 665–671.
    [Google Scholar]
  23. Schachtele, C. F. & Jensen, M. E. ( 1982; ). Comparison of methods for monitoring changes in the pH of human dental plaque. J Dent Res 61, 1117–1125.[CrossRef]
    [Google Scholar]
  24. Schwabacher, H., Lucas, D. R. & Rimmington, C. ( 1947; ). Bacterium melaninogenicum – a misnomer. J Gen Microbiol 1, 109–120.[CrossRef]
    [Google Scholar]
  25. Shah, H. N. & Williams, R. A. D. ( 1987; ). Utilization of glucose and amino acids by Bacteroides intermedius and Bacteroides gingivalis. Curr Microbiol 15, 241–246.[CrossRef]
    [Google Scholar]
  26. Shah, H. N., Williams, R. A. D., Bowden, G. H. & Hardie, J. M. ( 1976; ). Comparison of the properties of Bacteroides melaninogenicus from human dental plaque and other sites. J Appl Bacteriol 41, 473–492.[CrossRef]
    [Google Scholar]
  27. Shah, H. N., Bonnett, R., Mateen, B. & Williams, R. A. D. ( 1979; ). The porphyrin pigmentation of subspecies of Bacteroides melaninogenicus. Biochem J 180, 45–50.
    [Google Scholar]
  28. Silver, J. & Lukas, B. ( 1983; ). Mössbauer studies on protoporphyrin IX iron(III) solutions. Inorg Chim Acta 78, 219–224.[CrossRef]
    [Google Scholar]
  29. Smalley, J. W., Silver, J., Marsh, P. J. & Birss, A. J. ( 1998; ). The periodontopathogen Porphyromonas gingivalis binds iron protoporphyrin IX in the μ-oxo dimeric form: an oxidative buffer and possible pathogenic mechanism. Biochem J 331, 681–685.
    [Google Scholar]
  30. Smalley, J. W., Birss, A. J. & Silver, J. ( 2000; ). The periodontal pathogen Porphyromonas gingivalis harnesses the chemistry of the μ-oxo bishaem of iron protoporphyrin IX to protect against hydrogen peroxide. FEMS Microbiol Lett 183, 159–164.
    [Google Scholar]
  31. Smalley, J. W., Birss, A. J., Withnall, R. & Silver, J. ( 2002; ). Interactions of Porphyromonas gingivalis with oxyhaemoglobin and deoxyhaemoglobin. Biochem J 362, 239–245.[CrossRef]
    [Google Scholar]
  32. Takahashi, N. & Schachtele, C. F. ( 1990; ). Effect of pH on growth and proteolytic activity of Porphyromonas gingivalis and Bacteroides intermedia. J Dent Res 69, 1266–1269.[CrossRef]
    [Google Scholar]
  33. Takahashi, N. & Yamada, T. ( 2000; ). Glucose metabolism by Prevotella intermedia and Prevotella nigrescens. Oral Microbiol Immunol 15, 188–195.[CrossRef]
    [Google Scholar]
  34. Takahashi, N., Saito, K., Schachtele, C. F. & Yamada, T. ( 1997; ). Acid tolerance and acid-neutralizing activity of Porphyromonas gingivalis, Prevotella intermedia and Fusobacterium nucleatum. Oral Microbiol Immunol 12, 323–328.[CrossRef]
    [Google Scholar]
  35. Willcox, M. D. & Drucker, D. B. ( 1988; ). Partial characterisation of the inhibitory substances produced by Streptococcus oralis and related species. Microbios 55, 135–145.
    [Google Scholar]
  36. Withnall, R., Silver, J., Fern, G. & Smalley, J. W. ( 1999; ). Raman spectra of the black-pigmenting anaerobic bacterium, Porphyromonas gingivalis. In Spectroscopy of Biological Molecules, pp. 573–574. Edited by J. Greve, G. J. Puppels & C. Otto. Dordrecht: Kluwer.
  37. Zwickel, J., Weiss, E. I. & Schejter, A. ( 1992; ). Degradation of native hemoglobin following hemolysis by Prevotella loescheii. Infect Immun 60, 1721–1723.
    [Google Scholar]
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