1887

Microbiology Society logo

Volume 148, Issue 1

Killing of spores of by peroxynitrite appears to be caused by membrane damage Free

Abstract

During an infection of a higher eukaryote, dormant spores of a species have been previously shown to be present in cells that can generate the toxic agent peroxynitrite (PON). Dormant spores of were much more resistant to killing by PON than were growing cells, and spore-coat alteration or removal greatly decreased PON resistance. Spores were not killed by PON through DNA damage and lost no dipicolinic acid (DPA) during PON treatment. However, PON-killed spores lost DPA during subsequent heat treatments that caused much less DPA release from untreated spores. Although dead, the PON-killed spores germinated and initiated metabolism but never went through outgrowth; the great majority of germinated PON-killed spores also took up propidium iodide, indicating that they had suffered significant membrane damage and were dead. Together these data suggest that spore killing by PON is through some type of damage to the spore’s inner membrane.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): DPA, dipicolinic acid , membrane damage , PON, peroxynitrite , SASP, small acid-soluble protein , spore killing and spore resistance
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-1-307
2002-01-01
2024-05-12
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/1/1480307a.html?itemId=/content/journal/micro/10.1099/00221287-148-1-307&mimeType=html&fmt=ahah

References

  1. Bagyan I., Noback M., Bron S., Paidhungat M., Setlow P. 1998; Characterization of yhcN , a new forespore-specific gene of Bacillus subtilis . Gene 212:179–188 [CrossRef]
     [Google Scholar]
  2. Beckman J. S., Koppenol W. H. 1996; Nitric oxide, superoxide, and peroxynitrite: the good the bad and the ugly. Am J Physiol 271:C1424–C1437
     [Google Scholar]
  3. Beckman J. S., Chen J., Ischiropoulus H., Crow J. P. 1994; Oxidative chemistry of peroxynitrite. Methods Enzymol 233:229–240
     [Google Scholar]
  4. Bloomfield S. F., Arthur M. 1994; Mechanisms of inactivation and resistance of spores to chemical biocides. J Appl Bacteriol 76:91S–104S [CrossRef]
     [Google Scholar]
  5. Brunnelli L., Crow J. P., Beckman J. S. 1995; The comparative toxicity of nitric oxide and peroxynitrite to Escherichia coli . Arch Biochem Biophys 316:327–334 [CrossRef]
     [Google Scholar]
  6. Bryk R., Griffin P., Nathan C. 2000; Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407:205–211
     [Google Scholar]
  7. Buchanan C. E., Neyman S. L. 1986; Correlation of penicillin-binding protein composition with different functions of two membranes in Bacillus subtilis forespores. J Bacteriol 165:498–503
     [Google Scholar]
  8. Casillas-Martinez L., Setlow P. 1997; Alkyl hydroperoxide reductase, catalase, MrgA, and superoxide dismutase are not involved in resistance of Bacillus subtilis spores to heat or oxidizing agents. J Bacteriol 179:7420–7425
     [Google Scholar]
  9. Chen L., Xie Q., Nathan C. 1998; Alkyl hydroperoxide reductase subunit C (AhpC) protects bacterial and human cells against reactive nitrogen intermediates. Mol Cell 1:795–805 [CrossRef]
     [Google Scholar]
  10. Ciarciaglini G., Hill P. J., Davies K., McClure P. J., Kilsby D., Brown M. H., Coote P. J. 2000; Germination-induced bioluminescence, a route to determine the inhibitory effect of a combination preservation treatment on bacterial spores . Appl Environ Microbiol 66:3735–3742 [CrossRef]
     [Google Scholar]
  11. Driks A. 1999; The Bacillus subtilis spore coat. Microbiol Mol Biol Rev 63:1–20
     [Google Scholar]
  12. Driks A., Setlow P. 1999; Morphogenesis and properties of the bacterial spore. In Prokaryotic Development pp 191–218 Edited by Brun Y. V. Shimkets L. J. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  13. Fairhead H., Setlow B., Setlow P. 1993; Prevention of DNA damage in spores and in vitro by small, acid-soluble proteins from Bacillus species. J Bacteriol 175:1367–1374
     [Google Scholar]
  14. Flowers R. S., Martin S. E., Ordal Z. J. 1977; Catalase and enumeration of stressed Staphylococcus aureus cells. Appl Environ Microbiol 33:1112–1117
     [Google Scholar]
  15. Gadelha F. R., Thomson L., Fagian M. M., Costa A. D., Radi R., Vercesi A. E. 1997; Ca2+-independent permeabilization of the inner mitochondrial membrane by peroxynitrite is mediated by membrane protein thiol cross-linking and lipid peroxidation. Arch Biochem Biophys 345:243–250 [CrossRef]
     [Google Scholar]
  16. Gerhardt P., Scherrer R., Black S. H. 1972; Molecular sieving by dormant spore structures. In Spores V pp 68–74 Edited by Halvorson H. O. Hanson R., Campbell L. L. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  17. Guidi-Rontani C., Weber-Levy M., Labruyere E., Mock M. 1999; Germination of Bacillus anthracis spores within alveolar macrophages. Mol Microbiol 31:17–19
     [Google Scholar]
  18. Hill P. J., Hall L., Vinicombe D. A., Soper C. J., Setlow P., Waites W. M., Denyer S., Stewart G. S. A. B. 1994; Bioluminescence and spores as biological indicators of inimical processes. J Appl Bacteriol 76:129S–134S [CrossRef]
     [Google Scholar]
  19. Hood A. M., Tuck A., Dane C. R. 1990; A medium for the isolation, enumeration and rapid presumptive identification of injured Clostridium perfringens and Bacillus cereus. J Appl Bacteriol 69:359–372 [CrossRef]
     [Google Scholar]
  20. Hozz N., Darley-Usmar V. M., Wilson M. T., Moncada S. 1992; Production of hydroxyl radicals from the simultaneous generation of superoxide and nitric oxide. Biochem J 281:419–424
     [Google Scholar]
  21. Hurst J. K., Lymar S. V. 1997; Toxicity of peroxynitrite and related reactive nitrogen species toward Escherichia coli . Chem Res Toxicol 10:802–810 [CrossRef]
     [Google Scholar]
  22. Karp M. 1989; Expression of bacterial luciferase genes from Vibrio harveyi in Bacillus subtilis and in Escherichia coli. Biochim Biophys Acta 1007:84–90 [CrossRef]
     [Google Scholar]
  23. Keyer K., Imlay J. A. 1997; Inactivation of dehydratase [4Fe-4S] clusters and disruption of iron homeostasis upon cell exposure to peroxynitrite. J Biol Chem 272:27652–27659 [CrossRef]
     [Google Scholar]
  24. Khairutdinov R. F., Coddington J. W., Hurst J. K. 2000; Permeation of phospholipid membranes by peroxynitrite. Biochemistry 39:14238–14249 [CrossRef]
     [Google Scholar]
  25. Kuwahara H., Miyamoto Y., Akaike T., Kubota T., Sawa T., Okamoto S., Maeda H. 2000; Helicobacter pylori suppresses bactericidal activity of peroxynitrite via carbon dioxide production. Infect Immun 68:4378–4383 [CrossRef]
     [Google Scholar]
  26. Loshon C. A., Melly E., Setlow B., Setlow P. 2001; Analysis of the killing of spores of Bacillus subtilis by a new disinfectant, Sterilox® . J Appl Microbiol 91:1051–1058 [CrossRef]
     [Google Scholar]
  27. McDonnell G., Russell A. D. 1999; Antiseptics and disinfectants: activity, action and resistance development. Clin Microbiol Rev 12:147–179
     [Google Scholar]
  28. Mallozzi C., Stasi A. M., Minetti M. 1997; Peroxynitrite modulates tyrosine-dependent signal transduction pathway of human erythrocyte band 3. FASEB J 11:1281–1290
     [Google Scholar]
  29. Middleton A. M., Chadwick M. V., Sanderson J., Gaya H. 2000; Comparison of a solution of super-oxidized water (Sterilox) with glutaraldehyde for the disinfection of bronchoscopes, contaminated in vivo with Mycobacterium tuberculosis and Mycobacterium avium-intracellulare in sputum. J Hosp Infect 45:278–282 [CrossRef]
     [Google Scholar]
  30. Murray T., Popham D. L., Pearson C. B., Hand A. R., Setlow P. 1998; Analysis of the outgrowth of Bacillus subtilis spores lacking penicillin-binding protein 2a. J Bacteriol 180:6493–6502
     [Google Scholar]
  31. Nicholson W. L., Setlow P. 1990; Sporulation, germination and outgrowth. In Molecular Biological Methods for Bacillus pp 391–450 Edited by Harwood C. R. Cutting S. M. Chichester: Wiley;
     [Google Scholar]
  32. Nicholson W. L., Munakata N., Horneck G., Melosh H. J., Setlow P. 2000; Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64:548–572 [CrossRef]
     [Google Scholar]
  33. Paidhungat M., Setlow P. 2001; Spore germination and outgrowth. In Bacillus subtilis and its Relatives: From Genes to Cells Edited by Hoch J. A. Losick R., Sonenshein A. L. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  34. Paidhungat M., Setlow B., Driks A., Setlow P. 2000; Characterization of spores of Bacillus subtilis which lack dipicolinic acid. J Bacteriol 182:5505–5512 [CrossRef]
     [Google Scholar]
  35. Perrin D., Koppenol W. H. 2000; The quantitative oxidation of methionine to methionine sulfoxide by peroxynitrite. Arch Biochem Biophys 377:266–272 [CrossRef]
     [Google Scholar]
  36. Popham D. L., Helin J., Costello C. E., Setlow P. 1996; Muramic lactam in peptidoglycan of Bacillus subtilis spores is required for spore outgrowth but not for spore dehydration or heat resistance. Proc Natl Acad Sci USA 93:15405–15410 [CrossRef]
     [Google Scholar]
  37. Rotman Y., Fields M. L. 1967; A modified reagent for dipicolinic acid analysis. Anal Biochem 22:168
     [Google Scholar]
  38. Routledge M. N. 2000; Mutations induced by reactive nitrogen oxide species in the supF forward mutation assay. Mutat Res 450:95–105 [CrossRef]
     [Google Scholar]
  39. Russell A. D. 1982 The Destruction of Bacterial Spores pp 62–64 London: Academic Press;
     [Google Scholar]
  40. Russell A. D. 1990; Bacterial spores and chemical sporicidal agents. Clin Microbiol Rev 3:99–119
     [Google Scholar]
  41. Selkon J. B., Babb R. B., Morris R. 1999; Evaluation of the antimicrobial activity of a new super-oxidized water, Sterilox®, for the disinfection of endoscopes. J Hosp Infect 41:59–70 [CrossRef]
     [Google Scholar]
  42. Setlow B., Setlow P. 1980; Measurements of the pH within dormant and germinated bacterial spores. Proc Natl Acad Sci USA 77:2474–2476 [CrossRef]
     [Google Scholar]
  43. Setlow B., Setlow P. 1996; Role of DNA repair in Bacillus subtilis spore resistance. J Bacteriol 178:3486–3495
     [Google Scholar]
  44. Setlow B., McGinnis K. A., Ragkousi K., Setlow P. 2000; Effects of major spore-specific DNA binding proteins on Bacillus subtilis sporulation and spore properties. J Bacteriol 182:6906–6912 [CrossRef]
     [Google Scholar]
  45. Setlow B., Melly E., Setlow P. 2001; Properties of spores of Bacillus subtilis blocked at an intermediate stage in spore germination. J Bacteriol 183:4894–4899 [CrossRef]
     [Google Scholar]
  46. Setlow P. 1994; Mechanisms which contribute to the long-term survival of spores of Bacillus species. J Appl Bacteriol 23:49S–60S
     [Google Scholar]
  47. Setlow P. 2000; Resistance of bacterial spores. In Bacterial Stress Responses pp 217–230 Edited by Storz G. Hengge-Aronis R. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  48. Shetty N., Srinivasan S., Holton J., Ridgway C. L. 1999; Evaluation of microbiocidal activity of a new disinfectant: Sterilox® 2500 against Clostridium difficile spores, Helicobacter pylori , vancomycin resistant Enterococcus species, Candida albicans and several mycobacterial species. J Hosp Infect 41:101–105 [CrossRef]
     [Google Scholar]
  49. Soszynski M., Bartosz G. 1996; Effect of peroxynitrite on erythrocytes. Biochim Biophys Acta 1291:107–114 [CrossRef]
     [Google Scholar]
  50. Spek E. J., Wright T. L., Stitt H. S., Taghizadeh N. R., Tannenbaum S. R., Marinus M. G., Engelward B. P. 2001; Recombinational repair is critical for survival of Escherichia coli exposed to nitric oxide. J Bacteriol 183:131–138 [CrossRef]
     [Google Scholar]
  51. Tennen R., Setlow B., Davis K. L., Loshon C. A., Setlow P. 2000; Mechanisms of killing of spores of Bacillus subtilis by iodine, glutaraldehyde and nitrous acid. J Appl Microbiol 89:330–338 [CrossRef]
     [Google Scholar]
  52. Williams N. D., Russell A. D. 1993a; Revival of biocide-treated spores of Bacillus subtilis . J Appl Bacteriol 75:69–75 [CrossRef]
     [Google Scholar]
  53. Williams N. D., Russell A. D. 1993b; Revival of Bacillus subtilis spores from biocide-induced injury in the germination process. J Appl Bacteriol 75:76–81 [CrossRef]
     [Google Scholar]
  54. Yasbin R. E., Cheo D., Bol D. 1993; DNA repair systems. In Bacillus subtilis and Other Gram Positive Bacteria: Biochemistry, Physiology and Molecular Genetics pp 529–538 Edited by Sonenshein A. L. Hoch J. A., Losick R. Washington, DC: American Society for Microbiology;
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-1-307
Loading
Killing of spores of Bacillus subtilis by peroxynitrite appears to be caused by membrane damage
Microbiology 148, 307 (2002); https://doi.org/10.1099/00221287-148-1-307
/content/journal/micro/10.1099/00221287-148-1-307
/content/journal/micro/10.1099/00221287-148-1-307
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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