Spores of Bacillus subtilis: Their resistance to and killing by radiation, heat and chemicals

Journal of Applied Microbiology

Volumn 101, Issue 3, 2006, Pages 514-525

  Setlow, P ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; CELLS; CYTOLOGY; DIMERS; GAMMA RAYS; HEAT RESISTANCE; IRRADIATION; PROTEINS; REPAIR;

BACILLUS SPECIES; BACILLUS SUBTILIS; DNA DAMAGES; DNA-REPAIR; DRY HEAT; INNER MEMBRANES; PHOTOPRODUCTS; SPORE OUTGROWTH; Β'' TYPE; Γ-RADIATION;

DNA;

BACTERIAL DNA; BACTERIAL PROTEIN; CHEMICAL AGENT; COAT PROTEIN; CYCLOBUTANE; DIMER; DIPICOLINIC ACID; FORMALDEHYDE; ION; MINERAL; NITROUS ACID; OXIDIZING AGENT; PHOTOPROTEIN; PYRIMIDINE; SMALL ACID SOLUBLE SPORE PROTEIN; SMALL ACID SOLUBLE SPORE PROTEIN ALPHA; SMALL ACID SOLUBLE SPORE PROTEIN BETA; SPORE DNA; UNCLASSIFIED DRUG; WATER;

BACTERIUM; CHEMICAL COMPOUND; DNA; HEAT CAPACITY; ION; PROTEIN; RADIATION BUDGET; SPORE; ULTRAVIOLET RADIATION; WATER CONTENT;

BACILLUS; BACILLUS SUBTILIS; BACTERIAL ENDOSPORE; BACTERIAL MEMBRANE; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; CHEMICAL INJURY; CONFERENCE PAPER; DETOXIFICATION; DNA DAMAGE; DNA REPAIR; FOOD INDUSTRY; GAMMA RADIATION; HEAT; HEAT SENSITIVITY; HEAT TOLERANCE; INSTRUMENT STERILIZATION; MEDICAL INSTRUMENTATION; MEMBRANE PERMEABILITY; MEMBRANE RUPTURE; NONHUMAN; PHOTOCHEMISTRY; PHOTOSENSITIZATION; PROTEIN DNA BINDING; PROTOPLAST; SPORE GERMINATION; SPOROGENESIS; ULTRAVIOLET RADIATION; WATER CONTENT;

BACILLUS SUBTILIS;

EID: 33744733251     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2005.02736.x     Document Type: Conference Paper

References (75)

1. Ablett, S., Darke, A.H., Lillford, P.J. and Martin, D.R. (1999) Glass formation and dormancy in bacterial spores. Int J Food Sci Technol 34, 59-69.
2. Alderton, G. and Snell, N. (1969) Chemical states of bacterial spores: dry-heat resistance. Appl Microbiol 17, 745-749.
3. Bailey-Smith, K., Todd, S.J., Southworth, T.W., Proctor, J. and Moir, A. (2005) The ExsA protein of Bacillus cereus is required for assembly of coat and exosporium onto the spore surface. J Bacteriol 187, 3800-3806.
4. Bender, G.R. and Marquis, R.E. (1985) Spore heat resistance and specific mineralization. Appl Environ Microbiol 50, 1415-1421.
5. Cabrera-Martinez, R.-M., Setlow, B. and Setlow, P. (2002) Studies on the mechanism of the sporicidal action of ortho-phthalaldehyde. J Appl Microbiol 92, 675-680.
6. Cano, R.J. and Borucki, M. (1995) Revival and identification of bacterial spores in 25- to 40-million-year-old Dominican amber. Science 268, 1060-1064.
7. Casillas-Martinez, L. and 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.
8. Cheek, J. and Broderick, J.B. (2002) Direct H atom abstraction from spore photoproduct C-6 initiates DNA repair in the reaction catalyzed by spore photoproduct lyase: evidence for a reversibly generated adenosyl radical intermediate. J Am Chem Soc 124, 2860-2861.
9. Cortezzo, D.E. and Setlow, P. (2005) Analysis of factors influencing the sensitivity of spores of Bacillus subtilis to DNA damaging chemicals. J Appl Microbiol 98, 606-617.
10. Cortezzo, D.E., Koziol-Dube, K., Setlow, B. and Setlow, P. (2004) Treatment with oxidizing agents damages the inner membrane of spores of Bacillus subtilis and sensitizes the spores to subsequent stress. J Appl Microbiol 97, 838-852.
11. Cowan, A.E., Koppel, D.E., Setlow, B. and Setlow, P. (2003) A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores: implications for spore dormancy. Proc Natl Acad Sci U S A 100, 4209-4214.
12. Cowan, A.E., Olivastro, E.M., Koppel, D.E., Loshon, C.A., Setlow, B. and Setlow, P. (2004) Lipids in the inner membrane of dormant spores of Bacillus species are immobile. Proc Natl Acad Sci U S A 101, 7733-7738.
13. Daubenspeck, J.M., Zeng, H., Chen, P., Dong, S., Steichen, C.T., Krishna, N.R., Pritchard, D.G. and Turnbough, C.L. (2004) Novel oligosaccharide chains of the collagen-like region of BclA, the major glycoprotein of the Bacillus anthracis exosporium. J Biol Chem 279, 30945-30953.
14. Douki, T., Setlow, B. and Setlow, P. (2005a) Effects of the binding of α/β-type small, acid-soluble spore proteins on the photochemistry of DNA in spores of Bacillus subtilis and in vitro. Photochem Photobiol 81, 163-169.
15. Douki, T., Setlow, B. and Setlow, P. (2005b) Photosensitization of DNA by dipicolinic acid, a major component of spores of Bacillus species. Photochem Photobiol Sci 4, 591-597.
16. Driks, A. (1999) The Bacillus subtilis spore coat. Microbiol Mol Biol Rev 63, 1-20.
17. Driks, A. (2002a) Overview: development in bacteria: spore formation in Bacillus subtilis. Cell Mol Life Sci 59, 389-391.
18. Driks, A. (2002b) Proteins of the spore core and coat. In Bacillus subtilis and its Closest Relatives: from Genes to Cells ed. Sonenshein, A.L., Hoch, J.A. and Losick, R. pp. 527-535. Washington, DC: American Society for Microbiology.
19. Frenkiel-Krispin, D., Englander, J., Shimoni, E., Eisenstein, M., Bullitt, E., Horowitz-Scherer, R., Hayes, C.S., Setlow, P. et al. (2004) Structure of DNA-SspC complex: implications for DNA packaging, protection and repair in bacterial spores. J Bacteriol 186, 3525-3530.
20. Genest, P.C., Setlow, B., Melly, E. and Setlow, P. (2002) Killing of spores of Bacillus subtilis by peroxynitrite appears to be caused by membrane damage. Microbiology 148, 307-314.
21. Gerhardt, P. and Marquis, R.E. (1989) Spore thermoresistance mechanisms. In Regulation of Prokaryotic Development ed. Smith, I., Slepecky, R.A. and Setlow, P. pp. 43-63. Washington, DC: American Society for Microbiology.
22. Gerhardt, P., Scherrer, R. and Black, S.H. (1972) Molecular sieving by dormant spore structures. In Spores V ed. Halvorson, H.O., Hanson, R. and Campbell, L.L. pp. 68-74. Washington, DC: American Society for Microbiology.
23. Hayes, C.S. and Setlow, P. (2001) An α/β-type small, acid-soluble spore protein which has a very high affinity for DNA prevents outgrowth of Bacillus subtilis spores. J Bacteriol 183, 3982-3990.
24. Henriques, A.O., Melsen, L.R. and Moran, C.P. Jr (1998) Involvement of superoxide dismutase in spore coat assembly in Bacillus subtilis. J Bacteriol 180, 2285-2291.
25. del Huesca-Espita, L.C., Caley, C., Bagyan, I. and Setlow, P. (2002) Base-change mutations induced by various treatments of Bacillus subtilis spores with and without DNA protective small, acid-soluble spore proteins. Mutat Res 503, 77-84.
26. Kennedy, M.J., Reader, S.L. and Swierczynski, L.M. (1994) Preservation records of micro-organisms: evidence of the tenacity of life. Microbiology 140, 2513-2529.
27. Lai, E.M., Phadke, N.D., Kachman, M.T., Giorno, R., Vazquez, S., Vazquez, J.A., Maddock, J.R. and Driks, A. (2003) Proteomic analysis of the spore coats of Bacillus subtilis and Bacillus anthracis. J Bacteriol 185, 1443-1454.
28. Leuschner, R.G.K. and Lillford, P.J. (2000) Effects of hydration on molecular mobility in phase bright Bacillus subtilis spores. Microbiology 146, 49-55.
29. Leuschner, R.G.K. and Lillford, P.J. (2003) Thermal properties of bacterial spores and biopolymers. Int J Food Microbiol 80, 131-143.
30. Loshon, C.A., Genest, P.C., Setlow, B. and Setlow, P. (1999) Formaldehyde kills spores of Bacillus subtilis by DNA damage and small, acid-soluble spore proteins of the α/β-type protect against this DNA damage. J Appl Microbiol 87, 8-14.
31. Loshon, C.A., Melly, E., Setlow, B. and Setlow, P. (2001) Analysis of killing of spores of Bacillus subtilis by a new disinfectant, Sterilox®. J Appl Microbiol 91, 1051-1058.
32. McDonnell, G. and Russell, A.D. (1999) Antiseptics and resistance: activity, action and resistance. Clin Microbiol Rev 12, 147-179.
33. Mehl, R.A. and Begley, T.P. (1999) Mechanistic studies on the repair of a novel photolesion: the spore photoproduct. Org Lett 1, 1065-1066.
34. Melly, E. and Setlow, P. (2001) Heat shock proteins do not influence wet heat resistance of Bacillus spores. J Bacteriol 183, 779-784.
35. Melly, E., Cowan, A.E. and Setlow, P. (2002a) Studies on the mechanism of killing of Bacillus subtilis spores by hydrogen peroxide. J Appl Microbiol 93, 316-325.
36. Melly, E., Genest, P.C., Gilmore, M.E., Little, S., Popham, D.L., Driks, A. and Setlow, P. (2002b) Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. J Appl Microbiol 92, 1105-1115.
37. Nicholson, W.L., Munakata, N., Horneck, G., Melosh, H.J. and Setlow, P. (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64, 548-572.
38. Nicholson, W.L., Setlow, B. and Setlow, P. (2003) UV photochemistry of DNA in vitro and in Bacillus subtilis spores at earth-ambient and low atmospheric pressure: implications for spore survival on other planets or moons in the solar system. Astrobiology 2, 417-425.
39. Nicholson, W.L., Schuerger, A.C. and Setlow, P. (2005) The solar UV environment and bacterial spore UV resistance: considerations for Earth-to-Mars transport by natural processes and human spaceflight. Mutat Res 571, 249-264.
40. Paidhungat, M., Setlow, B., Driks, A. and Setlow, P. (2000) Characterization of spores of Bacillus subtilis which lack dipicolinic acid. J Bacteriol 182, 5505-5512.
41. Patrick, M.H. and Gray, D.M. (1976) Independence of photoproduct formation on DNA conformation. Photochem Photobiol 24, 507-513.
42. Piggot, P.J. and Hilbert, D.W. (2004) Sporulation of Bacillus subtilis. Curr Opin Microbiol 7, 579-586.
43. Popham, D.L. (2002) Specialized peptidogycan of the bacterial endospore: the inner wall of the lockbox. Cell Mol Life Sci 59, 426-433.
44. Rahn, R.O. and Hosszu, J.L. (1969) Influence of relative humidity on the photochemistry of DNA films. Biochim Biophys Acta 190, 126131.
45. Rebeil, R. and Nicholson, W.L. (2001) The subunit structure and catalytic mechanism of the Bacillus subtilis repair enzyme spore photoproduct lyase. Proc Natl Acad Sci U S A 98, 9038-9043.
46. Redmond, C., Baillie, L.W., Hibbs, S., Moir, A.J. and Moir, A. (2004) Identification of proteins in the exosporium of Bacillus anthracis. Microbiology 150, 355-363.
47. Riesenman, P.J. and Nicholson, W.L. (2000) Role of the spore coat layers in Bacillus subtilis resistance to hydrogen peroxide, artificial UV-C, UV-B, and solar radiation. Appl Environ Microbiol 66, 620-666.
48. Russell, A.D. (1982) The Destruction of Bacterial Spores. London: Academic Press.
49. Sanchez-Salas, J.-L., Santiago-Lara, M.L., Setlow, B., Sussman, M.D. and Setlow, P. (1992) Properties of mutants of Bacillus megaterium and Bacillus subtilis which lack the protease that degrades small, acid-soluble proteins during spore germination. J Bacteriol 174, 807-814.
50. Setlow, P. (1983) Germination and outgrowth. In The Bacterial Spore, Vol. II ed. Hurst, A. and Gould, G.W. pp. 211-254. London: Academic Press.
51. Setlow, P. (1992) I will survive: protecting and repairing spore DNA. J Bacteriol 174, 2737-2741.
52. Setlow, P. (1994) Mechanisms which contribute to the longterm survival of spores of Bacillus species. J Appl Bacteriol 76, 49S-60S.
53. Setlow, P. (1995) Mechanisms for the prevention of damage to the DNA in spores of Bacillus species. Annu Rev Microbiol 49, 29-54.
54. Setlow, P. (2000) Resistance of bacterial spores. In Bacterial Stress Responses ed. Storz, G. and Hengge-Aronis, R. pp. 217-230. Washington, DC: American Society for Microbiology.
55. Setlow, P. (2003) Spore germination. Curr Opinion Microbiol 6, 550-556.
56. Setlow, B. and Setlow, P. (1980) Measurements of the pH within dormant and germinated bacterial spores. Proc Natl Acad Sci USA 77, 2474-2476.
57. Setlow, B. and Setlow, P. (1995) Small, acid-soluble proteins bound to DNA protect Bacillus subtilis spores from killing by dry heat. Appl Environ Microbiol 61, 2787-2790.
58. Setlow, B. and Setlow, P. (1996) Role of DNA repair in Bacillus subtilis spore resistance. J Bacteriol 178, 3486-3495.
59. Setlow, B., Tautvydas, K.J. and Setlow, P. (1998) Small, acid-soluble spore proteins of the α/β-type do not protect the DNA in Bacillus subtilis spores against base alkylation. Appl Environ Microbiol 64, 1958-1962.
60. Setlow, B., McGinnis, K.A., Ragkousi, K. and Setlow, P. (2000) Effects of major spore-specific DNA binding proteins on Bacillus subtilis sporulation and spore properties. J Bacteriol 182, 6906-6912.
61. Setlow, B., Loshon, C.A., Genest, P.C., Cowan, A.E., Setlow, C. and Setlow, P. (2002) Mechanisms of killing of spores of Bacillus subtilis by acid, alkali and ethanol. J Appl Microbiol 92, 362-375.
62. Setlow, B., Cowan, A.E. and Setlow, P. (2003) Germination of spores of Bacillus subtilis with dodecylamine. J Appl Microbiol 95, 637-648.
63. 2 and ascorbic acid. Appl Environ Microbiol 70, 2535-2539.
64. Sohail, A., Hayes, C.S., Divvela, P., Setlow, P. and Bhagwat, A.S. (2002) Protection of DNA by α/β-type small, acid-soluble proteins from Bacillus subtilis spores against cytosine deamination. Biochemistry 41, 11325-11330.
65. + and other monovalent cations in dormant and germinated spores of Bacillus megaterium. J Bacteriol 148, 20-29.
66. Tennen, R., Setlow, B., Davis, K.L., Loshon, C.A. and Setlow, P. (2000) Mechanisms of killing of spores of Bacillus subtilis by iodine, glutaraldehyde and nitrous acid. J Appl Microbiol 89, 330-338.
67. Todd, S.J., Moir, A.J., Johnson, M.J. and Moir, A. (2003) Genes of Bacillus cereus and Bacillus anthracis encoding proteins of the exosporium. J Bacteriol 185, 3373-3378.
68. Vreeland, R.H., Rosenzweig, W.D. and Powers, D.W. (2000) Isolation of a 250 million-year old halotolerant bacterium from a primary salt crystal. Nature 407, 897-900.
69. Waller, L.N., Fox, N., Fox, K.F., Fox, A. and Price, R.L. (2004) Ruthenium red staining for ultrastructural visualization of a glycoprotein layer surrounding the spore of Bacillus anthracis and Bacillus subtilis. J Microbiol Methods 58, 23-30.
70. Warth, A.D. (1980) Heat stability of Bacillus cereus enzymes within spores and in extracts. J Bacteriol 143, 27-34.
71. Weller, G.R., Kysela, B., Roy, R., Tonkin, L.M., Scanlan, E., Della, M., Krogh Devine, S., Day, J.P. et al. (2002) Identification of a nonhomologous end-joining complex in bacteria. Science 297, 1686-1689.
72. Westphal, A.J., Price, B.P., Leighton, T.J. and Wheeler, K.E. (2003) Kinetics of size changes of individual Bacillus thuringiensis spores in response to changes in relative humidity. Proc Natl Acad Sci USA 100, 3461-3466.
73. Young, S.B. and Setlow, P. (2003) Mechanisms of killing of Bacillus subtilis spores by hypochlorite and chlorine dioxide. J Appl Microbiol 95, 54-67.
74. Young, S.B. and Setlow, P. (2004a) Mechanisms of killing of Bacillus subtilis spores by Decon and Oxone™, two general decontaminants for biological agents. J Appl Microbiol 96, 289-301.
75. Young, S.B. and Setlow, P. (2004b) Mechanisms of Bacillus subtilis spore resistance to and killing by aqueous ozone. J Appl Microbiol 96, 1133-1142.