Resistance of Bacterial Spores to Chemical Agents

Russell, Hugo & Ayliffe's: Principles and Practice of Disinfection, Preservation and Sterilization

Volumn , Issue , 2012, Pages 121-130

  Setlow, Peter ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Bacillales and Clostridiales; Bacterial spores; Spore purity; Spore resistance; Spore structure; Sporicide; Sporulation conditions

Indexed keywords

EID: 84887164215     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781118425831.ch6b     Document Type: Chapter

References (94)

1. Bloomfield, S.F. (1999) Bacterial sensitivity and resistance: resistance of bacterial spores to chemical agents, in Principles and Practice of Disinfection, Preservation and Sterilization, 3rd edn (eds A.D. Russell et al.), Blackwell Science, London, pp. 303-320
2. Setlow, P. (2006) Spores of Bacillus subtilis: their resistance to radiation, heat and chemicals. Journal of Applied Microbiology, 101, 514-525.
3. Setlow, P. and Johnson, E.A. (2007) Spores and their significance, in Food Microbiology, Fundamentals and Frontiers, 3rd edn (eds M.P. Doyle and L.R. Beuchat), ASM Press, Washington, DC, pp. 35-67
4. Russell, A.D. (2003) Similarities and differences in the responses of microorganisms to biocides. Journal of Antimicrobial Chemotherapy, 52, 750-763.
5. Russell, A.D. (2001) Mechanisms of bacterial insusceptibility to biocides. American Journal of Infection Control, 29, 259-261.
6. McDonnell, G. and Russell, A.D. (1999) Antiseptics and disinfectants: activity, action and resistance. Clinical Microbiology Reviews, 12, 147-179.
7. Brown, K.L. (2000) Control of bacterial spores. British Medical Bulletin, 56, 158-171.
8. Nicholson, W.L. et al. (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiology and Molecular Biology Reviews, 64, 548-572.
9. Maillard, J.-Y. (2011) Innate resistance to sporicides and potential failure to decontaminate. Journal of Hospital Infection, 77, 204-209.
10. Driks, A. (2009) The Bacillus anthracis spore. Molecular Aspects of Medicine, 30, 368-373.
11. Henriques, A.O. and Moran, C.P. Jr. (2007) Structure, assembly, and function of the spore surface layers. Annual Review of Microbiology, 61, 555-588.
12. Severson, K.M. et al. (2009) Roles of Bacillus anthracis spore protein ExsK in exosporium maturation and germination. Journal of Bacteriology, 191, 7587-7596.
13. Chesnokova, O.N. Jr. et al. (2009) The spore-specific alanine racemase of Bacillus anthracis and its role in suppressing germination during spore development. Journal of Bacteriology, 191, 1303-1310.
14. Cybulski, R.J. et al. (2009) Four superoxide dismutases contribute to Bacillus anthracis virulence and provide spores with redundant protection from oxidative stress. Infection and Immunity, 77, 274-285.
15. Klobutcher, L.A. et al. (2006) The Bacillus subtilis spore coat provides "eat resistance" during phagosomal predation by the protozoan Tetrahymena thermophila. Proceedings of the National Academy of Sciences of the United States of America, 103, 165-170.
16. Laaberki, M.H. and Dworkin, J. (2008) Role of spore coat proteins in the resistance of Bacillus subtilis spores to Caenorhabditis elegans predation. Journal of Bacteriology, 190, 6197-6203.
17. Popham, D.L. (2002) Specialized peptidoglycan of the bacterial endospore: the inner wall of the lockbox. Cellular and Molecular Life Sciences, 59, 426-433.
18. Swerdlow, B.M. et al. (1981) Levels of H+ and other monovalent cations in dormant and germinated spores of Bacillus megaterium. Journal of Bacteriology, 148, 20-29.
19. Sunde, E.P. et al. (2009) The physical state of water in bacterial spores. Proceedings of the National Academy Sciences of the United States of America, 106, 19334-19339.
20. Cortezzo, D.E. and Setlow, P. (2005) Analysis of factors influencing the sensitivity of spores of Bacillus subtilis to DNA damaging chemicals. Journal of Applied Microbiology, 98, 606-617.
21. Cowan, A.E. et al. (2004) Lipids in the inner membrane of dormant spores of Bacillus species are immobile. Proceedings of the National Academy of Sciences of the United States of America, 101, 7733-7738.
22. Griffiths, K. and Setlow, P. (2009) Effects of modification of membrane lipid composition on Bacillus subtilis sporulation and spore properties. Journal of Applied Microbiology, 106, 1600-1607.
23. Gerhardt, P. and Marquis, R.E. (1989) Spore thermoresistance mechanisms, in Regulation of Prokaryotic Development: Structural and Functional Analysis of Bacterial Sporulation and Germination (eds I. Smith et al.), American Society for Microbiology, Washington, DC, pp. 43-64
24. Paidhungat, M. et al. (2000) Characterization of spores of Bacillus subtilis which lack dipicolinic acid. Journal of Bacteriology, 182, 5505-5512.
25. Setlow, B. et al. (2006) Role of dipicolinic acid in the resistance and stability of spores of Bacillus subtilis. Journal of Bacteriology, 188, 3740-3747.
26. Setlow, P. (2007) I will survive: DNA protection in bacterial spores. Trends in Microbiology, 15, 172-180.
27. Cowan, A.E. et al. (2003) A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores: implications for spore dormancy. Proceedings of the National Academy of Sciences of the United States of America, 100, 4209-4214.
28. Sapru, V. and Labuza, T.P. (1993) Glassy state in bacterial spores predicted by polymer glass-transition theory. Journal of Food Science, 58, 445-448.
29. Ablett, S. et al. (1999) Glass formation and dormancy in bacterial spores. International Journal of Food Science and Technology, 34, 59-69.
30. Stecchini, M.L. et al. (2006) Glassy state in Bacillus subtilis spores analyzed by differential scanning calorimetry. International Journal of Food Microbiology, 106, 286-290.
31. Leuschner, R.G.K. and Lillford, P.J. (2003) Thermal properties of bacterial spores and biopolymers. International Journal of Food Microbiology, 80, 131-143.
32. Hornstra, L.M. et al. (2009) On the origin of heterogeneity in (preservation) resistance of Bacillus spores: input for a "systems" analysis approach of bacterial spore outgrowth. International Journal of Food Microbiology, 134, 9-15.
33. Zhang, P. et al. (2010) Characterization of wet heat inactivation of single spores of Bacillus species by dual-trap Raman spectroscopy and elastic light scattering. Applied and Environmental Microbiology, 76, 507-514.
34. Ghosh, S. et al. (2009) Superdormant spores of Bacillus species have elevated wet heat resistance and temperature requirements for heat activation. Journal of Bacteriology, 191, 5584-5591.
35. Ghosh, S. and Setlow, P. (2009) Isolation and characterization of superdormant spores of Bacillus species. Journal of Bacteriology, 191, 1787-1797.
36. Ghosh, S. and Setlow, P. (2010) The preparation, germination properties and stability of superdormant spores of Bacillus cereus. Journal of Applied Microbiology, 108, 582-590.
37. Rose, R. et al. (2007) Comparison of the properties of Bacillus subtilis spores made in liquid or on plates. Journal of Applied Microbiology, 103, 691-699.
38. Marquis, R.E. and Shin, S.Y. (1994) Mineralization and responses of bacterial spores to heat and oxidative agents. FEMS Microbiology Reviews, 14, 375-379.
39. Cazemier, A.E. et al. (2001) Effect of sporulation and recovery medium on the heat resistance and amount of injury of spores from spoilage bacilli. Journal of Applied Microbiology, 90, 761-770.
40. Melly, E. et al. (2002) Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. Journal of Applied Microbiology, 92, 1105-1115.
41. Baron, P.A. et al. (2007) Bacterial endospore inactivation caused by outgassing of vapourous hydrogen peroxide from polymethyl methacrylate (Plexiglas). Letters in Applied Microbiology, 45, 485-490.
42. Williams, N.D. and Russell, A.D. (1993) Revival of biocide-treated spores of Bacillus subtilis. Journal of Applied Bacteriology, 75, 69-75.
43. Williams, N.D. and Russell, A.D. (1993) Revival of Bacillus subtilis spores from biocide-induced injury in the germination process. Journal of Applied Bacteriology, 75, 76-81.
44. Setlow, B. et al. (2002) Mechanisms of killing of spores of Bacillus subtilis by acid, alkali and ethanol. Journal of Applied Microbiology, 92, 362-375.
45. Coleman, W.H. and Setlow, P. (2009) Analysis of damage due to moist heat treatment of spores of Bacillus subtilis. Journal of Applied Microbiology, 106, 1600-1607.
46. Warth, A.D. (1980) Heat stability of Bacillus cereus enzymes within spores and in extracts. Journal of Bacteriology, 143, 27-34.
47. Coleman, W.H. et al. (2007) How moist heat kills spores of Bacillus subtilis. Journal of Bacteriology, 189, 8458-8466.
48. Palop, A. et al. (1996) Hydroperoxide inactivation of enzymes within spores of Bacillus megaterium ATCC19213. FEMS Microbiology Letters, 44, 283-287.
49. Palop, A. et al. (1998) Inactivation of enzymes within spores of Bacillus mega-terium ATCC19213 by hydroperoxides. Canadian Journal of Microbiology, 44, 465-470.
50. Cabrera-Martinez, R.M. et al. (2002) Studies on the mechanisms of the spori-cidal action of o-phthalaldehyde. Journal of Applied Microbiology, 92, 675-680.
51. Walsh, S.E. et al. (1999) Ortho-phthalaldehyde: a possible alternative to glutar-aldehyde for high level disinfection. Journal of Applied Microbiology, 86, 1039-1046.
52. Melly, E. et al. (2002) Studies on the mechanism of killing of Bacillus subtilis spores by hydrogen peroxide. Journal of Applied Microbiology, 93, 316-325.
53. Cortezzo, D.E. et al. (2004) Treatment with oxidizing agents damages the inner membrane of spores of Bacillus subtilis and sensitizes the spores to subsequent stress. Journal of Applied Microbiology, 97, 838-852.
54. Young, S.B. and Setlow, P. (2003) Mechanisms of killing of Bacillus subtilis spores by hypochlorite and chlorine dioxide. Journal of Applied Microbiology, 95, 54-67.
55. Young, S.B. and Setlow, P. (2004) Mechanisms of Bacillus subtilis spore resistance to and killing by aqueous ozone. Journal of Applied Microbiology, 96, 1133-1142.
56. Loshon, C.A. et al. (2001) Analysis of killing of spores of Bacillus subtilis by a new disinfectant, Sterilox®. Journal of Applied Microbiology, 91, 1051-1058.
57. Hurst, A. (1977) Bacterial injury: a review. Canadian Journal of Microbiology, 23, 935-944.
58. Hurst, A. (1983) Injury, in The Bacterial Spore, vol. II, (eds A. Hurst and G.W. Gould), Academic Press, London, pp. 255-274
59. Shitani, H. (2006) Importance of considering injured microorganisms in sterilization validation. Biocontrol Science, 11, 91-106.
60. Imlay, J.A. (2008) Cellular defenses against superoxide and hydrogen peroxide. Annual Review of Biochemistry, 77, 755-776.
61. Imlay, J.A. (2003) Pathways of oxidative damage. Annual Review of Microbiology, 57, 395-418.
62. Casillas-Martinez, L. and Setlow, P. (1997) Alkyl hydroperoxide reductase, cata-lase, MrgA, and superoxide dismutase are not involved in resistance of Bacillus subtilis spores to heat or oxidizing agents. Journal of Bacteriology, 179, 7420-7425.
63. Setlow, B. et al. (1998) Small, acid-soluble spore proteins of the α/β-type do not protect the DNA in Bacillus subtilis spores against base alkylation. Applied and Environmental Microbiology, 64, 1958-1962.
64. Lee, K.S. et al. (2007) Structure of a protein-DNA complex essential for DNA protection in spores of Bacillus species. Proceedings of the National Academy of Sciences of the United States of America, 105, 2806-2811.
65. Loshon, C.A. et al. (1999) Formaldehyde kills spores of Bacillus subtilis by DNA damage, and small, acid-soluble spore proteins of the α/β-type protect spores against this DNA damage. Journal of Applied Microbiology, 87, 8-14.
66. Tennen, R. et al. (2000) Mechanisms of killing of spores of Bacillus subtilis by iodine, glutaraldehyde and nitrous acid. Journal of Applied Microbiology, 89, 330-338.
67. Setlow, B. et al. (1997) Killing bacterial spores by organic hydroperoxides. Journal of Industrial Microbiology, 18, 384-388.
68. Setlow, B. and Setlow, P. (1993) Binding of small, acid-soluble spore proteins to DNA plays a significant role in the resistance of Bacillus subtilis spores to hydrogen peroxide. Applied and Environmental Microbiology, 59, 3418-3423.
69. Bayliss, C.E. and Waites, W.M. (1979) The combined effect of hydrogen peroxide and ultraviolet irradiation on bacterial spores. Journal of Applied Bacteriology, 47, 263-269.
70. Reidmiller, J.S. et al. (2003) Characterization of UV-peroxide killing of bacterial spores. Journal of Food Protection, 66, 1233-1240.
71. Young, S.B. and Setlow, P. (2004) Mechanisms of killing of Bacillus subtilis spores by Decon and Oxone™, two general decontaminants for biological agents. Journal of Applied Microbiology, 96, 289-301.
72. Bosak, T. et al. (2008) A polycyclic terpenoid that alleviates oxidative stress. Proceedings of the National Academy of Sciences of the United States of America, 105, 6725-6729.
73. Ghosh, S. et al. (2011) Effects of Mn levels on resistance of Bacillus megaterium spores to heat, radiation and hydrogen peroxide. Journal of Applied Microbiology, 111, 663-670.
74. 2+, other divalent cations, orthophosphate, and dipi-colinic acid on protein resistance to ionizing radiation. Applied and Environmental Microbiology, 77, 32-40.
75. Collins, T.J. and Walter, C. (2006) Little green molecules. Scientific American, 294, 82-90.
76. Paul, M. et al. (2007) Killing of spores of Bacillus subtilis by tert-butyl hydroperoxide plus a TAML activator. Journal of Applied Microbiology, 102, 954-962.
77. Paul, M. et al. (2006) Mechanisms of killing of spores by dimethyldioxirane. Journal of Applied Microbiology, 101, 1161-1168.
78. Riesenman, P.J. and Nicholson, W.L. (2000) Role of the spore coat layers in Bacillus subtilis spore resistance to hydrogen peroxide, artificial UV-C, UV-B, and solar UV radiation. Applied and Environmental Microbiology, 66, 620-626.
79. Ghosh, S. et al. (2008) Characterization of spores of Bacillus subtilis that lack most coat layers. Journal of Bacteriology, 190, 6741-6748.
80. Yardimci, O. and Setlow, P. (2010) Plasma sterilization: opportunities and microbial assessment strategies in medical device manufacturing. IEEE Transactions in Plasma Science, 38, 973-981.
81. Langsrud, S. et al. (2000) Potentiation of the lethal effect of peroxygen on Bacillus cereus spores by alkali and enzyme wash. International Journal of Food Microbiology, 56, 81-86.
82. Hirota, R. et al. (2009) The silicon layer supports acid resistance of Bacillus cereus spores. Journal of Bacteriology, 192, 111-116.
83. Robinow, C. (1953) Spore structure as revealed by thin sections. Journal of Bacteriology, 66, 300-311.
84. Roth, S. et al. (2010) Characterization of Bacillus subtilis spore inactivation in low-pressure, low-temperature gas plasma sterilization processes. Journal of Applied Microbiology, 108, 521-531.
85. Zhang, J. et al. (2006) Sterilizing Bacillus pumilus spores using supercritical carbon dioxide. Journal of Microbiological Methods, 66, 479-485.
86. Hemmer, J.D. et al. (2007) Sterilization of bacterial spores by using supercritical carbon dioxide and hydrogen peroxide. Journal of Biomedical Materials Research B: Applied Biomaterials, 80, 511-518.
87. Zhang, J. et al. (2007) Supercritical carbon dioxide and hydrogen peroxide cause mild changes in spore structures associated with high killing rate of Bacillus anthracis. Journal of Microbiological Methods, 70, 442-451.
88. Shieh, E. et al. (2009) Sterilization of Bacillus pumilus spores using supercritical fluid carbon dioxide containing various modifier solutions. Journal of Microbiological Methods, 76, 247-252.
89. Li, J. and McClane, B.A. (2008) A novel small acid soluble protein variant is important for spore resistance of most Clostridium perfringens food poisoning isolates. Public Library of Science Pathology, 4, e1000056.
90. Li, J. et al. (2009) Further characterization of Clostridium perfringens small acid soluble protein-4 (Ssp4) properties and expression. Public Library of Science One, 4, e6249.
91. Paredes-Sabja, D. et al. (2008) Role of small, acid-soluble spore proteins in the resistance of Clostridium perfringens spores to chemicals. International Journal of Food Microbiology, 122, 333-335.
92. Leyva-Illades, J.F. et al. (2007) Effect of a small, acid-soluble spore protein from Clostridium perfringens on the resistance properties of Bacillus subtilis spores. Journal of Bacteriology, 189, 7927-7931.
93. Parades-Sabja, D. et al. (2008) Roles of DacB and Spm proteins in Clostridium perfringens spore resistance to moist heat and chemicals. Applied and Environmental Microbiology, 74, 3730-3738.
94. Paredes-Sabja, D. et al. (2008) Characterization of Clostridium perfringens spores that lack SpoVA proteins and dipicolinic acid. Journal of Bacteriology, 190, 4648-4659.