Skip to main content
PMC home page
The British Journal of Venereal Diseases logoLink to The British Journal of Venereal Diseases
. 1984 Feb;60(1):14–22. doi: 10.1136/sti.60.1.14

Susceptibility of Treponema pallidum to the toxic products of oxygen reduction and the non-treponemal nature of its catalase.

B Steiner, G H Wong, S Graves
PMCID: PMC1046263  PMID: 6421449

Abstract

We examined the sensitivity of Treponema pallidum (Nichols strain) to toxic products of oxygen reduction. T pallidum was sensitive to hydrogen peroxide at concentrations similar to those to which obligate anaerobes are sensitive. Accelerated death of T pallidum occurred at hydrogen peroxide concentrations below 50 mumol/l. Agents protective against hydrogen peroxide and the hydroxyl free radical (catalase, peroxidase, and mannitol) significantly enhanced treponemal survival in vitro under all three conditions of aerobiosis tested--that is, air, 3% oxygen, and 3% oxygen in conjunction with a reduced medium. Superoxide dismutase (which provides protection against superoxide radicals) did not enhance treponemal survival in normal media. When superoxide radicals were generated in the medium by means of a xanthine and xanthine oxidase system, however, the enzyme did protect T pallidum. A possible toxic involvement of singlet oxygen was also indicated by enhanced treponemal survival in air in the presence of histidine. Extracts of T pallidum from infected rabbit testes showed catalase activity which, on polyacrylamide gel electrophoresis, had the same relative mobility as purified rabbit catalase. The treponemal catalase activity was neutralised by anti rabbit catalase antiserum (raised in guinea pigs). This confirmed that the catalase was of rabbit origin and not an endogenous enzyme of T pallidum. We discuss the relation of these results to the obligate parasitism of T pallidum.

Full text

PDF
16

Images in this article

20Image
on p.20

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ananthaswamy H. N., Eisenstark A. Repair of hydrogen peroxide-induced single-strand breaks in Escherichia coli deoxyribonucleic acid. J Bacteriol. 1977 Apr;130(1):187–191. doi: 10.1128/jb.130.1.187-191.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Austin F. E., Barbieri J. T., Corin R. E., Grigas K. E., Cox C. D. Distribution of superoxide dismutase, catalase, and peroxidase activities among Treponema pallidum and other spirochetes. Infect Immun. 1981 Aug;33(2):372–379. doi: 10.1128/iai.33.2.372-379.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Azar H. A., Pham T. D., Kurban A. K. An electron microscopic study of a syphilitic chancre. Engulfment of Treponema pallidum by plasma cells. Arch Pathol. 1970 Aug;90(2):143–150. [PubMed] [Google Scholar]
  4. BEERS R. F., Jr, SIZER I. W. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem. 1952 Mar;195(1):133–140. [PubMed] [Google Scholar]
  5. Barbieri J. T., Cox C. D. Influence of oxygen on respiration and glucose catabolism by Treponema pallidum. Infect Immun. 1981 Mar;31(3):992–997. doi: 10.1128/iai.31.3.992-997.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Baseman J. B., Nichols J. C., Mogerley S. Capacity of virulent Treponema pallidum (Nichols) for deoxyribonucleic acid synthesis. Infect Immun. 1979 Feb;23(2):392–397. doi: 10.1128/iai.23.2.392-397.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brause B. D., Qualls S., Roberts R. B. Testicular cultivation of Treponema pallidum (Nichols strains) facilitated by sustained-release steroid administration. J Clin Microbiol. 1979 Dec;10(6):937–939. doi: 10.1128/jcm.10.6.937-939.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brawn K., Fridovich I. DNA strand scission by enzymically generated oxygen radicals. Arch Biochem Biophys. 1981 Feb;206(2):414–419. doi: 10.1016/0003-9861(81)90108-9. [DOI] [PubMed] [Google Scholar]
  9. Carlsson J., Carpenter V. S. The recA+ gene product is more important than catalase and superoxide dismutase in protecting Escherichia coli against hydrogen peroxide toxicity. J Bacteriol. 1980 Apr;142(1):319–321. doi: 10.1128/jb.142.1.319-321.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carlsson J., Granberg G. P., Nyberg G. K., Edlund M. B. Bactericidal effect of cysteine exposed to atmospheric oxygen. Appl Environ Microbiol. 1979 Mar;37(3):383–390. doi: 10.1128/aem.37.3.383-390.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Carlsson J., Nyberg G., Wrethén J. Hydrogen peroxide and superoxide radical formation in anaerobic broth media exposed to atmospheric oxygen. Appl Environ Microbiol. 1978 Aug;36(2):223–229. doi: 10.1128/aem.36.2.223-229.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev. 1979 Jul;59(3):527–605. doi: 10.1152/physrev.1979.59.3.527. [DOI] [PubMed] [Google Scholar]
  13. Cohen G. The generation of hydroxyl radicals in biologic systems: toxicological aspects. Photochem Photobiol. 1978 Oct-Nov;28(4-5):669–675. doi: 10.1111/j.1751-1097.1978.tb06993.x. [DOI] [PubMed] [Google Scholar]
  14. Cox C. D., Barber M. K. Oxygen uptake by Treponema pallidum. Infect Immun. 1974 Jul;10(1):123–127. doi: 10.1128/iai.10.1.123-127.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. DAVIS B. J. DISC ELECTROPHORESIS. II. METHOD AND APPLICATION TO HUMAN SERUM PROTEINS. Ann N Y Acad Sci. 1964 Dec 28;121:404–427. doi: 10.1111/j.1749-6632.1964.tb14213.x. [DOI] [PubMed] [Google Scholar]
  16. Dempsey P. M., O'Leary J., Condon S. Polarographic assay of hydrogen peroxide accumulation in microbial cultures. Appl Microbiol. 1975 Feb;29(2):170–174. doi: 10.1128/am.29.2.170-174.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fieldsteel A. H., Becker F. A., Stout J. G. Prolonged survival of virulent Treponema pallidum (Nichols strain) in cell-free and tissue culture systems. Infect Immun. 1977 Oct;18(1):173–182. doi: 10.1128/iai.18.1.173-182.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fieldsteel A. H., Cox D. L., Moeckli R. A. Further studies on replication of virulent Treponema pallidum in tissue cultures of Sf1Ep cells. Infect Immun. 1982 Feb;35(2):449–455. doi: 10.1128/iai.35.2.449-455.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Finn G. J., Condon S. Regulation of catalase synthesis in Salmonella typhimurium. J Bacteriol. 1975 Aug;123(2):570–579. doi: 10.1128/jb.123.2.570-579.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fitzgerald T. J., Johnson R. C. Surface mucopolysaccharides of Treponema pallidum. Infect Immun. 1979 Apr;24(1):244–251. doi: 10.1128/iai.24.1.244-251.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fitzgerald T. J., Johnson R. C., Wolff E. T. Sulfhydryl oxidation using procedures and experimental conditions commonly used for Treponema pallidum. Br J Vener Dis. 1980 Jun;56(3):129–136. doi: 10.1136/sti.56.3.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fitzgerald T. J., Miller J. N., Sykes J. A. Treponema pallidum (Nichols strain) in tissue cultures: cellular attachment, entry, and survival. Infect Immun. 1975 May;11(5):1133–1140. doi: 10.1128/iai.11.5.1133-1140.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Fridovich I. Oxygen: boon and bane. Am Sci. 1975 Jan-Feb;63(1):54–59. [PubMed] [Google Scholar]
  24. Graves S. R., Sandok P. L., Jenkin H. M., Johnson R. C. Retention of motility and virulence of Treponema pallidum (Nichols strain) in vitro. Infect Immun. 1975 Nov;12(5):1116–1120. doi: 10.1128/iai.12.5.1116-1120.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Halliwell B. Superoxide-dependent formation of hydroxyl radicals in the presence of iron salts. Its role in degradation of hyaluronic acid by a superoxide-generating system. FEBS Lett. 1978 Dec 15;96(2):238–242. doi: 10.1016/0014-5793(78)80409-8. [DOI] [PubMed] [Google Scholar]
  26. Harley J. B., Santangelo G. M., Rasmussen H., Goldfine H. Dependence of Escherichia coli hyperbaric oxygen toxicity on the lipid acyl chain composition. J Bacteriol. 1978 Jun;134(3):808–820. doi: 10.1128/jb.134.3.808-820.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Harmon S. M., Kautter D. A. Beneficial effect of catalase treatment on growth of Clostridium perfringens. Appl Environ Microbiol. 1976 Sep;32(3):409–416. doi: 10.1128/aem.32.3.409-416.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  29. Lysko P. G., Cox C. D. Terminal electron transport in Treponema pallidum. Infect Immun. 1977 Jun;16(3):885–890. doi: 10.1128/iai.16.3.885-890.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Marklund S., Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 1974 Sep 16;47(3):469–474. doi: 10.1111/j.1432-1033.1974.tb03714.x. [DOI] [PubMed] [Google Scholar]
  31. McCord J. M., Keele B. B., Jr, Fridovich I. An enzyme-based theory of obligate anaerobiosis: the physiological function of superoxide dismutase. Proc Natl Acad Sci U S A. 1971 May;68(5):1024–1027. doi: 10.1073/pnas.68.5.1024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Murray H. W., Cohn Z. A. Macrophage oxygen-dependent antimicrobial activity. I. Susceptibility of Toxoplasma gondii to oxygen intermediates. J Exp Med. 1979 Oct 1;150(4):938–949. doi: 10.1084/jem.150.4.938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Norris S. J., Miller J. N., Sykes J. A., Fitzgerald T. J. Influence of oxygen tension, sulfhydryl compounds, and serum on the motility and virulence of Treponema pallidum (Nichols strain) in a cell-free system. Infect Immun. 1978 Dec;22(3):689–697. doi: 10.1128/iai.22.3.689-697.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Norris S. J., Miller J. N., Sykes J. A. Long-term incorporation of tritiated adenine into deoxyribonucleic acid and ribonucleic acid by Treponema pallidum (Nichols strain). Infect Immun. 1980 Sep;29(3):1040–1049. doi: 10.1128/iai.29.3.1040-1049.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Olsen J., Davis L. The oxidation of dithiothreitol by peroxidases and oxygen. Biochim Biophys Acta. 1976 Sep 14;445(2):324–329. doi: 10.1016/0005-2744(76)90086-3. [DOI] [PubMed] [Google Scholar]
  36. Rolfe R. D., Hentges D. J., Campbell B. J., Barrett J. T. Factors related to the oxygen tolerance of anaerobic bacteria. Appl Environ Microbiol. 1978 Aug;36(2):306–313. doi: 10.1128/aem.36.2.306-313.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. STRITTMATTER C. F. Flavin-linked oxidative enzymes of Lactobacillus casei. J Biol Chem. 1959 Oct;234:2794–2800. [PubMed] [Google Scholar]
  38. Schiller N. L., Cox C. D. Catabolism of glucose and fatty acids by virulent Treponema pallidum. Infect Immun. 1977 Apr;16(1):60–68. doi: 10.1128/iai.16.1.60-68.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Steiner B., McLean I., Graves S. Redox potential and survival of virulent Treponema pallidum under microaerophilic conditions. Br J Vener Dis. 1981 Oct;57(5):295–301. doi: 10.1136/sti.57.5.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Woodbury W., Spencer A. K., Stahman M. A. An improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem. 1971 Nov;44(1):301–305. doi: 10.1016/0003-2697(71)90375-7. [DOI] [PubMed] [Google Scholar]

Articles from British Journal of Venereal Diseases are provided here courtesy of BMJ Publishing Group

RESOURCES