Spore resistance properties

Microbiology Spectrum

Volumn 2, Issue 5, 2014, Pages

  Setlow, Peter ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; INORGANIC COMPOUND; ORGANIC COMPOUND;

BACILLUS; BACTERIAL SPORE; CHEMISTRY; CLOSTRIDIUM; DESICCATION; DRUG EFFECTS; HEAT; MICROBIAL VIABILITY; PHYSIOLOGY; RADIATION RESPONSE;

BACILLUS; CLOSTRIDIUM; DESICCATION; ENZYMES; HOT TEMPERATURE; INORGANIC CHEMICALS; MICROBIAL VIABILITY; ORGANIC CHEMICALS; SPORES, BACTERIAL;

EID: 84953910824     PISSN: None     EISSN: 21650497     Source Type: Journal    
DOI: 10.1128/microbiolspec.TBS-0003-2012     Document Type: Article

References (91)

1. Peck MW, Stringer SC, Carter AT. 2011. Clostridium botulinum in the post-genomic era. Food Microbiol 28:183-191.
2. Setlow P, Johnson EA. 2012. Spores and their significance, p 45-79. In Doyle MP, Bucanan R (ed), Food Microbiology: Fundamentals and Frontiers, 4th ed. ASM Press, Washington, DC.
3. Potot S, Serra CR, Henriques AO, Schyns G. 2010. Display of recombinant proteins on Bacillus subtilis spores, using a coat-associated enzyme as the carrier. Appl Environ Microbiol 76:5926-5933.
4. Bader J, Albin A, Stahl U. 2012. Spore-forming bacteria and their utilization as probiotics. Benef Microbes 3:67-75.
5. Coleman WH, Chen D, Li Y-q, Cowan AE, Setlow P. 2007. How moist heat kills spores of Bacillus subtilis. J Bacteriol 189:8458-8466.
6. Coleman WH, Zhang P, Li Yq, Setlow P. 2010. Mechanism of killing of spores of Bacillus cereus and Bacillus megaterium by wet heat. Lett Appl Microbiol 50:507-514.
7. Setlow B, Parish S, Zhang P, Li YQ, Neely C, Setlow P. 2014. Mechanism of killing of spores of Bacillus anthracis in a high-temperature gas environment, and analysis of DNA damage generated by various decontamination treatments of spores of Bacillus anthracis, Bacillus subtilis and Bacillus thuringiensis. J Appl Microbiol 116:805-814.
8. Brul, S, van Beilen J, Caspers M, O'Brien A, de Koster C, Oomes S, Smelt J, Kort R, Ter Beek A. 2011. Challenges and advances in systems biology analysis of Bacillus spore physiology; molecular differences between an extreme heat resistant spore forming Bacillus subtilis food isolate and a laboratory strain. Food Microbiol 28:221-227.
9. Leggett MJ, McDonnell G, Denyer SP, Setlow P, Maillard J-Y. 2012. Bacterial spore structures and their protective role in biocide resistance. J Appl Microbiol 113:485-499.
10. Maillard J-Y. 2011. Innate resistance to sporicides and potential failure to decontaminate. J Hosp Infect 77:204-209.
11. Setlow P. 2006. Spores of Bacillus subtilis: their resistance to radiation, heat and chemicals. J Appl Microbiol 101:514-525.
12. Setlow P. 2007. I will survive: DNA protection in bacterial spores. Trends Microbiol 15:172-180.
13. Setlow P. 2010. Resistance of bacterial spores, p 319-332. In Storz G, Hengge R (ed), Bacterial Stress Response, 2nd ed. American Society for Microbiology, Washington, DC.
14. Setlow P. 2012. Resistance of bacterial spores to chemical agents, p 121-130. In Maillard J-Y, Fraise A, Sattar S (ed), Principles and Practice of Disinfection, Preservation & Sterilization, 4th ed. Wiley-Blackwell, Oxford, United Kingdom.
15. Ter Beek A, Brul S. 2010. To kill or not to kill Bacilli: opportunities for food biotechnology. Curr Opin Biotechnol 21:168-174.
16. Henriques AO, Moran CP Jr. 2007. Structure, assembly, and function of the spore surface layers. Annu Rev Microbiol 61:555-588.
17. Klobutcher LA, Ragkousi K, Setlow P. 2006. The Bacillus subtilis spore coat provides "eat resistance" during phagosomal predation of the protozoan Tetrahymena thermophila. Proc Natl Acad Sci USA 103:165-170.
18. Laaberki MH, Dworkin J. 2008. Role of spore coat proteins in the resistance of Bacillus subtilis spores to Caenorhabditis elegans predation. J Bacteriol 190:197-203.
19. Bosak T, Losick RM, Pearson A. 2008. A polycyclic terpenoid that alleviates oxidative stress. Proc Natl Acad Sci USA 105:6725-6729.
20. Khaneja R, Perez-Fons L, Fakhry S, Baccigalupi L, Steiger S, To E, Sandmann G, Dong TC, Ricca E, Fraser PD, Cutting SM. 2010. Carotenoids found in Bacillus. J Appl Microbiol 108:1889-1902.
21. Griffiths KK, Setlow P. 2009. Effects of modification of membrane lipid composition on Bacillus subtilis sporulation and spore properties. J Appl Microbiol 106:2064-2078.
22. Cortezzo DE, Setlow P. 2005. Analysis of factors that influence the sensitivity of spores of Bacillus subtilis to DNA damaging chemicals. J Appl Microbiol 98:606-617.
23. Loisan P, Hosny NA, Gervais P, Champion D, Kuimova MK, Perrier-Cornet JM. 2013. Direct investigation of viscosity of an atypical inner membrane of Bacillus spores: a molecular rotor/FLIM study. Biochim Biophys Acta 1828:2436-2443.
24. Sunde EP, Setlow P, Hederstedt L, Halle B. 2009. The physical state of water in bacterial spores. Proc Natl Acad Sci USA 106:19334-19339.
25. Lee KS, Bumbaca D, Kosman J, Setlow P, Jedrzejas MJ. 2008. Structure of a protein-DNA complex essential for DNA protection in spores of Bacillus species. Proc Natl Acad Sci USA 105:2806-2811.
26. Fairhead H. 2009. SASP gene delivery: a novel antibacterial approach. Drug News Perspect 22:197-203.
27. Ramírez-Gaudiana FH, Barraza-Salas M, Ramírez-Ramírez N, Ortiz-Cortés M, Setlow P, Pedraza-Reyes M. 2012. Alternative excision repair of ultraviolet B-and C-induced DNA damage in dormant and developing spores of Bacillus subtilis. J Bacteriol 194:6096-6104.
28. Maclean M, Murdoch LE, MacGregor SJ, Anderson JG. 2013. Sporicidal effects of high-intensity 405 nm visible light on endospore-forming bacteria. Photochem Photobiol 89:120-126.
29. Tyler GSD, Dai T, Hamblin MR. 2013. Killing bacterial spores with blue light: when innate resistance meets the power of light. Photochem Photobiol 89:2-4.
30. Levy C, Aubert X, Lacour B, Carlin F. 2012. Relevant factors affecting microbial surface decontamination by pulsed light. Int J Food Microbiol 152:168-174.
31. Moeller R, Setlow P, Reitz G, Nicholson WL. 2009. Roles of small, acid-soluble spore proteins and core water content in survival of Bacillus subtilis spores exposed to environmental solar UV radiation. Appl Environ Microbiol 75:5202-5208.
32. Moeller R, Wassmann M, Reitz G, Setlow P. 2011. Effect of radioprotective agents in sporulation medium on Bacillus subtilis spore resistance to hydrogen peroxide, wet heat and germicidal and environmentally relevant UV radiation. J Appl Microbiol 110:1485-1494.
33. Ghosh S, Ramirez-Peralta A, Gaidamakova E, Zhang P, Li Y-Q, Daly MJ, Setlow P. 2011. Effects of Mn levels on resistance of Bacillus megaterium spores to heat, radiation and hydrogen peroxide. J Appl Microbiol 111:663-670.
34. Ibarra JR, Orozco AD, Rojas JA, Lopez K, Setlow P, Yasbin RE, Pedraza-Reyes M. 2008. Role of the Nfo and ExoA apurinic/apyrimidinic endonucleases in repair of DNA damage during outgrowth of Bacillus subtilis spores. J Bacteriol 190:2031-2038.
35. Moeller R, Setlow P, Pedraza-Reyes M, Okayasu R, Reitz G, Nicholson WL. 2011. Role of the Nfo and ExoA apurinic/apyrimidinic (AP) endonucleases in the radiation resistance and radiation-induced mutagenesis of Bacillus subtilis spores. J Bacteriol 193:2875-2879.
36. Chandra T, Silver SC, Zilinskas E, Shepard EM, Broderick WE, Broderick JB. 2009. Spore photoproduct lyase catalyzes specific repair of the 5R but not the 5S spore photoproduct. J Am Chem Soc 131:2420-2421.
37. Yang L, Nelson RS, Benjdia A, Lin G, Telser J, Stoll S, Schlichting I, Li L. 2013. A radical transfer pathway in spore photoproduct lyase. Biochemistry 52:3041-3050.
38. Li J, Paredes-Sabja D, Sarker MR, McClane BA. 2009. Further characterization of Clostridium perfringens small acid soluble protein-4 (Ssp4) properties and expression. PLoS One 4:e6249. doi: 10.1371/journal.pone.0006249.
39. Raju D, Walters M, Setlow P, Sarker MR. 2006. Investigating the role of small, acid-soluble spore proteins (SASPs) in the resistance of Clostridium perfringens spores to heat. BMC Microbiol 6:50. doi:10.1186/1471-2180-6-50.
40. Leyva-Illades JF, Setlow B, Sarker MR, Setlow P. 2007. Effect of a small, acid-soluble spore protein from Clostridium perfringens on the resistance properties of Bacillus subtilis spores. J Bacteriol 189:7927-7931.
41. Moeller R, Raguse M, Reitz G, Okayasu R, Li Z, Klein S, Setlow P, Nicholson WL. 2014. Resistance of Bacillis subtilis spore DNA to lethal ionizing radiation damage relies heavily on spore core components and DNA repair, with minor effects of oxygen radical detoxification. Appl Environ Microbiol 80:104-109.
42. Moeller R, Setlow P, Horneck G, Berger T, Reitz G, Rutberg P, Doherty AJ, Okayasu R, Nicholson WL. 2008. Role of major small, acid-soluble spore proteins, spore specific and universal DNA repair mechanisms in the resistance of Bacillus subtilis spores to ionizing radiation from X-rays and high energy charged (HZE) particle bombardment. J Bacteriol 190:1134-1140.
43. Vlasic I, Mertens R, Seco EM, Carrasco B, Ayora S, Reitz G, Commichau FM, Alonso JC, Moeller R. 2014. Bacillus subtilis RecA and its accessory factors, RecF, RecO, RecR and RecX, are required for spore resistance to DNA double-strand breaks. Nucleic Acids Res 42:2295-2307.
44. Checinska A, Burbank M, Paszczynski AJ. 2012. Protection of Bacillus pumilus spores by catalases. Appl Environ Microbiol 78:6413-6422.
45. Cybulski RJ Jr, Sanz P, Alem F, Stibitz S, Bull RL, O'Brien AD. 2009. Four superoxide dismutases contribute to Bacillus anthracis virulence and provide spores with redundant protection from oxidative stress. Infect Immun 77:274-285.
46. Cowan AE, Koppel DE, Setlow B, 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 USA 100:4209-4214.
47. Castellanos-Juarez FX, Alvarez-Alvarez C, Yasbin RE, Setlow B, Setlow P, Pedraza-Reyes M. 2006. YtkD and MutT protect vegetative cells but not spores of Bacillus subtilis from oxidative stress. J Bacteriol 188: 2285-2289.
48. Armas A de Benito, Padula NL, Setlow B, Setlow P. 2008. Sensitization of Bacillus subtilis spores to dry heat and desiccation by pre-treatment with oxidizing agents. Lett Appl Microbiol 46:492-497.
49. Hirota R, Hata Y, Ikeda T, Ishida T, Kuroda A. 2010. The silicon layer supports acid resistance of Bacillus cereus spores. J Bacteriol 192: 111-116.
50. Coleman WH, Setlow P. 2009. Analysis of damage due to moist heat treatment of spores of Bacillus subtilis. J Appl Microbiol 106:1600-1607.
51. Zhang P, Kong L, Setlow P, Li YQ. 2010. Characterization of wet heat inactivation of single spores of Bacillus species by dual-trap Raman spectroscopy and elastic light scattering. Appl Environ Microbiol 76: 1796-1805.
52. Zhang P, Kong L, Wang G, Setlow P, Li Y-Q. 2011. Monitoring the wet-heat inactivation dynamics of single spores of Bacillus species using Raman tweezers, differential interference contrast and nucleic acid dye fluorescence microscopy. Appl Environ Microbiol 77:4754-4769.
53. Barraza-Salas M, Ibarra-Rodriguez JR, Mellado SJ, Salas-Pacheco J-M, Setlow P, Pedraza-Reyes M. 2010. Effects of forespore-specific overexpression of apurinic/apyrimidinic-endonuclease Nfo on the DNAdamage resistance properties of Bacillus subtilis spores. FEMS Lett 302: 159-165.
54. Magge A, Granger AC, Wahome PG, Setlow B, Vepachedu VR, Loshon CA, Peng L, Chen D, Li Y-q, Setlow P. 2008. Role of dipicolinic acid in the germination, stability and viability of spores of Bacillus subtilis. J Bacteriol 190:4798-4807.
55. Granger AC, Gaidamakova EK, Matrosova VY, Daly MJ, Setlow P. 2011. Effects of levels of Mn and Fe on Bacillus subtilis spore resistance, and effects of Mn2+, other divalent cations, orthophosphate, and dipicolinic acid on resistance of a protein to ionizing radiation. Appl Environ Microbiol 77:32-40.
56. Paredes-Sabja D, Setlow B, Setlow P, Sarker MR. 2008. Characterization of Clostridium perfringens spores that lack SpoVA proteins and dipicolinic acid. J Bacteriol 190:4648-4659.
57. Mah JH, Kang DH, Tang J. 2008. Effects of minerals on sporulation and heat resistance of Clostridium sporogenes. Int J Food Microbiol 128:385-389.
58. Garcia D, van der Voort M, Abee T. 2010. Comparative analysis of Bacillus weihenstephanensis KBAB4 spores obtained at different temperatures. Int J Food Microbiol 140:146-153.
59. Huo Z, Zhang N, Raa W, Huang X, Yong X, Liu Y, Wang D, Li S, Shen Q, Zhang R. 2012. Comparison of the spores of Paenibacillus polymyxa prepared at different temperatures. Biotechnol Lett 34:925-933.
60. Mah JH, Kang DH, Tang J. 2009. Comparison of viability and heat resistance of Clostridium sporogenes stored at different temperatures. J Food Sci 74:M23-M27.
61. Planchon S, Dargaignaratz C, Levy C, Ginies C, Broussolle V, Carlin F. 2011. Spores of Bacillus cereus strain KBAB4 produced at 10°C and 30°C display variations in their properties. Food Microbiol 28:291-297.
62. Baril E, L. Coroller L, Couvert O, Leguerinel I, Postollec F, Boulais C, Carlin F, Mafart P. 2012. Modeling heat resistance of Bacillus weihenstephanensis and Bacillus licheniformis spores as function of sporulation temperature and pH. Food Microbiol 30:29-36.
63. Minh HNT, Durand A, Loison P, Perrier-Cornet J-M, Gervais P. 2011. Effect of sporulation conditions on the resistance of Bacillus subtilis spores to heat and high pressure. Appl Micro Cell Physiol 90: 1409-1417.
64. Rose R, Setlow B, Monroe A, Malozzi M, Driks A, Setlow P. 2007. Comparison of the properties of Bacillus subtilis spores made in liquid or on plates. J Appl Microbiol 103:691-699.
65. Stecchini ML, Spaziani M, Del Torre M, Pacor S. 2009. Bacillus cereus cell and spore properties as influenced by the micro-structure of the medium. J Appl Microbiol 106:1838-1848.
66. Orsburn B, Sucre K, Popham DL, Melville SB. 2009. The SpmA/B and DacF proteins of Clostridium perfringens play important roles in spore heat resistance. FEMS Microbiol Lett 291:188-194.
67. Paredes-Sabja D, Sarker N, Setlow B, Setlow P, Sarker M. 2008. Roles of DacB and Spm proteins in Clostridium perfringens spore resistance to moist heat and chemicals. Appl Environ Microbiol 74:3730-3738.
68. Popham DL, Sengupta S, Setlow P. 1995. Heat, hydrogen peroxide and UV resistance of Bacillus subtilis spores with an increased core water content and with or without major DNA-binding proteins. Appl Environ Microbiol 61:3633-3638.
69. Derossi A, Fiore AG, De Pilli T, Severini C. 2011. A review on acidifying treatments for vegetable canned food. Crit Rev Food Sci Nutr 51: 955-964.
70. Cabo ML, Torres B, Herrera JJ, Bernardez M, Pastoriza L. 2009. Application of nisin and pediocin against resistance and germination of Bacillus spores in sous vide products. J Food Prot 72:515-523.
71. Wang G, Zhang P, Setlow P, Li YQ. 2011. Kinetics of germination of wet heat-treated individual spores of Bacillus species as followed by Raman spectroscopy and differential interference contrast microscopy. Appl Environ Microbiol 77:3368-3379.
72. Eijlander RT, Abee T, Kuipers OP. 2011. Bacterial spores in food: how phenotypic variability complicates prediction of spore properties and bacterial behavior. Curr Opin Biotechnol 22:180-186.
73. Ghosh S, Zhang P, Li Y-q, Setlow P. 2009. Superdormant spores of Bacillus species have elevated wet heat resistance and temperature requirements for heat activation. J Bacteriol 191:5584-5591.
74. Hornstra LM, Ter Beek A, Smelt JP, Kallemeijn WW, Brul S. 2009. On the origin of heterogeneity in (preservation) resistance of Bacillus spores: Input for a 'systems' analysis approach of bacterial spore outgrowth. Int J Food Microbiol 134:9-15.
75. Rodriguez-Palacios A, Lejeune JT. 2011. Moist-heat resistance, spore aging, and superdormancy in Clostridium difficile. Appl Environ Microbiol 77:3085-3091.
76. Sanchez-Salas J-L, Setlow B, Zhang P, Li YQ, Setlow P. 2011. Maturation of released spores is necessary for acquisition of full spore heat resistance during Bacillus subtilis sporulation. Appl Environ Microbiol 77:6746-6754.
77. Setlow P. 2007. Germination of spores of Bacillus subtilis by high pressure, p 15-40. In Doona CJ, Feeherry FE (ed), High Pressure Processing of Foods. Wiley-Blackwell, Hoboken, NJ.
78. Georget E, Kapoor S, Winter R, Reineke K, Song Y, Callanan M, Ananta E, Heinz V, Mathys A. 2014. In situ investigation of Geobacillus stearothermophilus spore germination and inactivation mechanisms under moderate high pressure. Food Microbiol 41:8-18.
79. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64:548-572.
80. Reineke K, Mathys A, Heinz V, Knorr D. 2013. Mechanisms of endospore inactivation under high pressure. Trends Microbiol 21:296-304.
81. Reineke K, Schlumbach K, Baier D, Mathys A, Knorr D. 2013. The release of dipicolinic acid-the rate-limiting step of Bacillus endospore inactivation during the high pressure thermal sterilization process. Int J Food Microbiol 162:55-63.
82. Jones CA, Padula NL, Setlow P. 2005. Effect of mechanical abrasion on the viability, disruption and germination of spores of Bacillus subtilis. J Appl Microbiol 99:1484-1494.
83. Gates SD, McCartt AD, Jeffries JB, Hanson RK, Hokama LA, Mortelmans KE. 2011. Extension of Bacillus endospore gas dynamic heating studies to multiple species and test conditions. J Appl Microbiol 111:925-931.
84. Gates SD, McCartt AD, Lappas P, Jeffries JB, Hanson RK, Hokama LA, Mortelmans KE. 2010. Bacillus endospore resistance to gas dynamic heating. J Appl Microbiol 109:1591-1598.
85. Tseng S, Abramzon N, Jackson JO, Lin W-J. 2012. Gas discharge plasmas are effective in inactivating Bacillus and Clostridium species. Appl Microbiol Biotechnol 93:2563-2570.
86. Yardimci O, Setlow P. 2010. Plasma sterilization: opportunities and microbial assessment strategies in medical device manufacturing. IEEE Trans Plasma Sci 38:973-981.
87. Checinska A, Firth IA, Green TL, Crawford, RL Paszczynski AJ. 2011. Sterilization of biological pathogens using supercritical carbon dioxide containing water and hydrogen peroxide. J Microbiol Methods 87:70-75.
88. Shieh E, Paszczynski A, Wai CM, Lang Q, Crawford RL. 2009. Sterilization of Bacillus pumilus spores using supercritical fluid carbon dioxide containing various modifier solutions. J Microbiol Methods 76:247-252.
89. Setlow P, Liu J, Faeder JR. 2012. Heterogeneity in bacterial spore populations, p 201-216. In Abel-Santos E (ed), Bacterial Spores: Current Research and Applications. Horizon Scientific Press, Norwich, United Kingdom.
90. Segey E, Smith Y, Ben-Yehuda S. 2012. RNA dynamics in aging bacterial spores. Cell 148:139-149.
91. Isticato R, Ricca E. 2014. Spore surface display. Microbiol Spectrum 2(5):TBS-0011-2012.