Mechanisms of endospore inactivation under high pressure

Trends in Microbiology

Volumn 21, Issue 6, 2013, Pages 296-304

  Reineke, Kai ^a,b   Mathys, Alexander ^c   Heinz, Volker ^c   Knorr, Dietrich ^a  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^b LEIBNIZ INSTITUTE FOR AGRICULTURAL ENGINEERING AND BIOECONOMY ATB   (Germany)

^c German Institute of Food Technology   (Germany)

Author keywords

Endospore; Germination and inactivation mechanisms; High pressure thermal sterilization; Matrix interactions

Indexed keywords

HYDROGEN PEROXIDE; HYPOCHLORITE SODIUM; SODIUM CHLORITE;

ASEPSIS; BACILLUS; BACTERIAL ENDOSPORE; BACTERIAL ENDOSPORE INACTIVATION; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL SURVIVAL; CLOSTRIDIUM; DESICCATION; ENVIRONMENTAL TEMPERATURE; FOOD PRESERVATION; FOOD SAFETY; HEAT TOLERANCE; HEAT TREATMENT; HIGH PRESSURE THERMAL STERILIZATION; HIGH TEMPERATURE; HUMAN; IONIZING RADIATION; NONHUMAN; PRESSURE; PRIORITY JOURNAL; REVIEW; SPORE GERMINATION; STRUCTURAL GENE; ULTRAVIOLET RADIATION;

BACILLUS SUBTILIS; FOOD PRESERVATION; HOT TEMPERATURE; HYDROSTATIC PRESSURE; MICROBIAL VIABILITY; PICOLINIC ACIDS; SPORES, BACTERIAL; STERILIZATION;

EID: 84878461264     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2013.03.001     Document Type: Review

References (95)

1. Heinz V., Knorr D. Effects of high pressure on spores. Ultra High Pressure Treatments of Foods 2002, 77-114. Kluwer Academic/Plenum Publishers. M. Hendrickx, D. Knorr (Eds.).
2. Knorr D. High pressure processing for preservation, modification and transformation of foods. High Press. Res. 2002, 22:595-599.
3. Setlow P. Spore germination. Curr. Opin. Microbiol. 2003, 6:550-556.
4. Wei J., et al. Superdormant spores of Bacillus species germinate normally with high pressure, peptidoglycan fragments, and bryostatin. J. Bacteriol. 2010, 192:1455-1458.
5. Coleman W.H., et al. Mechanism of killing of spores of Bacillus cereus and Bacillus megaterium by wet heat. Lett. Appl. Microbiol. 2010, 50:507-514.
6. Tabit F.T., Buys E. The effects of wet heat treatment on the structural and chemical components of Bacillus sporothermodurans spores. Int. J. Food Microbiol. 2010, 140:207-213.
7. Sanchez-Salas J.L., et al. Maturation of released spores is necessary for acquisition of full spore heat resistance during Bacillus subtilis sporulation. Appl. Environ. Microbiol. 2011, 77:6746-6754.
8. Setlow P., et al. Heterogeneiy in bacterial spore populations. Bacterial Spores 2012, 199-214. Caister Academic Press. E. Abel-Santos (Ed.).
9. Robleto E.A., et al. Gene regulations of sporulation in Bacillus subtilis. Bacterial Spores 2012, 9-18. Caister Academic Press. E. Abel-Santos (Ed.).
10. Bacterial Spores - Current Research and Applications 2012, Caister Academic Press. E. Abel-Santos (Ed.).
11. Paredes-Sabja D., et al. Germination of spores of Bacillales and Clostridiales species: mechanisms and proteins involved. Trends Microbiol. 2011, 19:85-94.
12. Setlow P. Dynamics of the assembly of a complex macromolecular structure - the coat of spores of the bacterium Bacillus subtilis. Mol. Microbiol. 2012, 83:241-244.
13. Pedraza-Reyes M., et al. Mechanisms of bacterial spore survival. Bacterial Spores 2012, 73-88. Caister Academic Press. E. Abel-Santos (Ed.).
14. Dirks A. The Bacillus subtilis spore coat. Microbiol. Mol. Biol. Rev. 1999, 63:1-20.
15. Nicholson W.L., et al. Resistance of Bacillus endospores to extreme terrestial and extraterrestial environments. Microbiol. Mol. Biol. Rev. 2000, 64:549-560.
16. Cortezzo D.E., Setlow P. Analysis of factors that influence the sensitivity of spores of Bacillus subtilis to DNA damaging chemicals. J. Appl. Microbiol. 2005, 98:606-617.
17. Popham D.L. Specialized peptidoglycan of the bacterial endospore: the inner wall of the lockbox. Cell. Mol. Life Sci. 2002, 59:426-433.
18. Cowan A.E., et al. Lipids in the inner membrane of dormant spores of Bacillus species are largely immobile. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:7733-7738.
19. Sunde E.P., et al. The physical state of water in bacterial spores. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:19334-19339.
20. Setlow B., et al. Role of dipicolinic acid in resistance and stability of spores of Bacillus subtilis with or without DNA-protective alpha/beta-type small acid-soluble proteins. J. Bacteriol. 2006, 188:3740-3747.
21. Huang S.S., et al. Levels of Ca(2+)-dipicolinic acid in individual Bacillus spores determined using microfluidic raman tweezers. J. Bacteriol. 2007, 189:4681-4687.
22. Setlow P. I will survive: DNA protection in bacterial spores. Trends Microbiol. 2007, 15:172-180.
23. Lee K.S., et al. Structure of a protein-DNA complex essential for DNA protection in spores of Bacillus species. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2806-2811.
24. Nakayama A., et al. Comparison of pressure resistances of spores of six Bacillus strains with their heat resistances. Appl. Environ. Microbiol. 1996, 62:3897-3900.
25. Margosch D., et al. Comparison of pressure and heat resistance of Clostridium botulinum and other endospores in mashed carrots. J. Food Prot. 2004, 72:3476-3481.
26. Raso J., et al. Sporulation temperature affects initiation of germination and inactivation by high hydrostatic pressure of Bacillus cereus. J. Appl. Microbiol. 1998, 85:17-24.
27. Melly E., et al. Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. J. Appl. Microbiol. 2002, 92:1105-1115.
28. Minh H.N.T., et al. Effect of sporulation conditions on the resistance of Bacillus subtilis spores to heat and high pressure. J. Appl. Microbiol. Biotechnol. 2011, 90:1409-1417.
29. Kato M., Hayashi R. Effects of high pressure on lipids and biomembranes for understanding high-pressure-induced biological phenomena. Biosci. Biotechnol. Biochem. 1999, 63:1321-1328.
30. Black E.P., et al. Factors influencing germination of Bacillus subtilis spores via activation of nutrient receptors by high pressure. Appl. Environ. Microbiol. 2005, 71:5879-5887.
31. Igura N., et al. Effects of minerals on resistance of Bacillus subtilis spores to heat and hydrostatic pressure. Appl. Environ. Microbiol. 2003, 69:6307-6310.
32. Oh S., Moon M.J. Inactivation of Bacillus cereus spores by high hydrostatic pressure at different temperatures. J. Food Prot. 2003, 66:599-603.
33. Margosch D., et al. Pressure inactivation of Bacillus endospores. Appl. Environ. Microbiol. 2004, 70:7321-7328.
34. Abee T., et al. Germination and outgrowth of spores of Bacillus cereus group members: diversity and role of germinant receptors. Food Microbiol. 2011, 28:199-208.
35. Winter R., Jeworrek C. Effect of pressure on membranes. Soft Matter 2009, 5:3157-3173.
36. Juliano P., et al. C. botulinum inactivation kinetics implemented in a computational model of a high-pressure sterilization process. Biotechnol. Prog. 2009, 25:163-175.
37. Mathys A., et al. Impact of dissociation equilibrium shift on bacterial spore inactivation by heat and pressure. Food Control 2008, 19:1165-1173.
38. Mathys A., et al. Impact of agglomeration on the quantitative assessment of Bacillus stearothermophilus heat inactivation. J. Food Eng. 2007, 81:380-387.
39. Heinz V., Knorr D. High pressure inactivation kinetics of Bacillus subtilis cells by a three-state-model considering distribution resistance mechanisms. Food Biotechnol. 1996, 10:149-161.
40. Reineke K., et al. The release of dipicolinic acid - the rate-limiting step of Bacillus endospore inactivation during the high pressure thermal sterilization process. Int. J. Food Microbiol. 2013, 162:55-63.
41. Wuytack E.Y., et al. Comparative study of pressure-induced germination of Bacillus subtilis spores at low and high pressures. Appl. Environ. Microbiol. 1998, 64:3220-3224.
42. Mathys A., et al. Flow cytometric assessment of Bacillus spore response to high pressure and heat. Innovat. Food Sci. Emerg. Technol. 2007, 8:519-527.
43. Reineke K., et al. The different pathways of spore germination and inactivation in dependence of pressure and temperature. Innovat. Food Sci. Emerg. Technol. 2012, 13:31-41.
44. Gould G.W., Sale A.J.H. Initiation of germination of bacterial spores by hydrostatic pressure. J. Gen. Microbiol. 1970, 60:335-346.
45. Wuytack E.Y., et al. Comparative study of pressure- and nutrient-induced germination of Bacillus subtilis spores. Appl. Environ. Microbiol. 2000, 66:257-261.
46. Paidhungat M., et al. Mechanisms of induction of germination of Bacillus subtilis spores by high pressure. Appl. Environ. Microbiol. 2002, 68:3172-3175.
47. Ardia, A. (2004) Process considerations on the application of high pressure treatment at elevated temperature levels for food preservation, In Department of Food Biotechnology and Food Process Engineering, pp. 94, Berlin University of Technology.
48. Margosch D., et al. High-pressure-mediated survival of Clostridium botulinum and Bacillus amyloliquefaciens endospores at high temperature. Appl. Environ. Microbiol. 2006, 72:3476-3481.
49. Mathys A., et al. High pressure thermal sterilization - development and application of temperature controlled spore inactivation studies. High Press. Res. 2009, 29:3-7.
50. Reineke K., et al. Structural analysis of high pressure treated Bacillus subtilis spores. Innovat. Food Sci. Emerg. Technol. 2013, 17:43-53.
51. Christie G. Inition of germination in Bacillus and Clostridium spores. Bacterial Spores 2012, 89-106. Caister Academic Press. E. Abel-Santos (Ed.).
52. Wei J., et al. Effects of moderately high pressure plus heat on the germination and inactivation of Bacillus cereus spores lacking proteins involved in germination. Lett. Appl. Microbiol. 2009, 49:646-651.
53. Zhang P.F., et al. Factors affecting variability in time between addition of nutrient germinants and rapid dipicolinic acid release during germination of spores of Bacillus species. J. Bacteriol. 2010, 192:3608-3619.
54. Sale A.J.H., et al. Inactivation of bacterial spores by hydrostatic pressure. J. Gen. Microbiol. 1970, 60:323-334.
55. Smelt J.P., et al. Effects of high pressure on vegetative microorganisms. Ultra High Pressure Treatments of Foods 2001, 55-76. Kluwer Academic. M. Hendrickx, D. Knorr (Eds.).
56. 2+-dipicolinate. J. Bacteriol. 2001, 183:4886-4893.
57. Setlow B., et al. Germination of spores of Bacillus subtilis with dodecylamine. J. Appl. Microbiol. 2003, 95:637-648.
58. Paredes-Sabja D., et al. Role of GerKB in germination and outgrowth of Clostridium perfringens spores. Appl. Environ. Microbiol. 2009, 75:3813-3817.
59. Paredes-Sabja D., et al. The protease CspB is essential for initiation of cortex hydrolysis and dipicolinic acid (DPA) release during germination of spores of Clostridium perfringens type A food poisoning isolates. Microbiology 2009, 155:3464-3472.
60. Reineke K., et al. The impact of high pressure and temperature on bacterial spores: inactivation mechanisms of Bacillus subtilis above 500MPa. J. Food Sci. 2011, 76:M189-M197.
61. Rajan S., et al. Combined pressure-thermal inactivation kinetics of Bacillus amyloliquefaciens spores in egg patty mince. J. Food Prot. 2006, 69:853-860.
62. Bull M.K., et al. Synergistic inactivation of spores of proteolytic Clostridium botulinum strains by high pressure and heat is strain and product dependent. Appl. Environ. Microbiol. 2009, 75:434-445.
63. Olivier S.A., et al. Strong and consistently synergistic inactivation of spores of spoilage-associated Bacillus and Geobacillus spp. by high pressure and heat compared with inactivation by heat alone. Appl. Environ. Microbiol. 2011, 77:2317-2324.
64. Zhu S.M., et al. High-pressure destruction kinetics of Clostridium sporogenes spores in ground beef at elevated temperatures. Int. J. Food Microbiol. 2008, 126:86-92.
65. Ramaswamy H.S., Shao Y.W. High pressure destruction kinetics of Clostridium sporogenes spores in salmon slurry at elevated temperatures. Int. J. Food Prop. 2010, 13:1074-1091.
66. Ratphitagsanti W., et al. Efficacy of pressure-assisted thermal processing, in combination with organic acids, against Bacillus amyloliquefaciens spores suspended in deionized water and carrot puree. J. Food Sci. 2010, 75:M46-M52.
67. Marco A., et al. Effect of olive powder and high hydrostatic pressure on the inactivation of Bacillus cereus spores in a reference medium. Foodborne Pathog. Dis. 2011, 8:681-685.
68. Gao Y.L., et al. Assessment of Clostridium perfringens spore response to high hydrostatic pressure and heat with nisin. Appl. Biochem. Biotechnol. 2011, 164:1083-1095.
69. Gao Y.L., Ju X.R. Inactivation of Bacillus coagulans spores subjected to combinations of high-pressure processing and nisin. Transact. ASABE 2011, 54:385-392.
70. Wuytack E.Y., Michiels C.W. A study on the effects of high pressure and heat on Bacillus subtilis spores at low pH. Int. J. Food Microbiol. 2001, 64:333-341.
71. Vercammen A., et al. Germination and inactivation of Bacillus coagulans and Alicyclobacillus acidoterrestris spores by high hydrostatic pressure treatment in buffer and tomato sauce. Int. J. Food Microbiol. 2012, 152:162-167.
72. Raso J., et al. Influence of sporulation temperature on the heat resistance of a strain of Bacillus licheniformis (Spanish type culture collection 4523). Food Microbiol. 1995, 12:357-361.
73. Gerhardt P., Marquis R.E. Spore thermorsistance mechanims. Regulation of Procaryotic Development 1989, 43-63. American Society for Microbiology. I. Smith (Ed.).
74. del Huesca Espitia L.C., et al. Base-change mutations induced by various treatments of Bacillus subtilis spores with and without DNA protective small, acid-soluble spore proteins. Mutat. Res. 2002, 503:77-84.
75. Setlow P. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 2006, 101:514-525.
76. Salas-Pacheco J.A., et al. Role of the Nfo (YqfS) and ExoA apurinic/apyrimidinic endonucleases in protecting Bacillus subtilis spores from DNA damage. J. Bacteriol. 2005, 187:7374-7381.
77. Barraza-Salas M., et al. Effects of forespore-specific overexpression of apurinic/apyrimidinic endonuclease Nfo on the DNA-damage resistance properties of Bacillus subtilis spores. FEMS Microbiol. Lett. 2010, 302:159-165.
78. Setlow P. Mechanisms for the prevention of damage to DNA in spores of Bacillus species. Annu. Rev. Microbiol. 1995, 49:29-54.
79. Nicastro A.J., et al. Limits imposed by ionizing radiation on the long-term survival of trapped bacterial spores: beta radiation. Int. J. Radiat. Biol. 2002, 78:891-901.
80. 2+, other divalent cations, orthophosphate, and dipicolinic acid on protein resistance to ionizing radiation. Appl. Environ. Microbiol. 2011, 77:32-40.
81. Douki T., et al. Photosensitization of DNA by dipicolinic acid, a major component of spores of Bacillus species. Photochem. Photobiol. Sci. 2005, 4:591-597.
82. Douki T., et al. Effects of the binding of alpha/beta-type small, acid-soluble spore proteins on the photochemistry of DNA in spores of Bacillus subtilis and in vitro. Photochem. Photobiol. 2005, 81:163-169.
83. Pelczar P.L., Setlow P. Localization of the germination protein GerD to the inner membrane in Bacillus subtilis spores. J. Bacteriol. 2008, 190:5635-5641.
84. Pelczar P.L., et al. Role of GerD in germination of Bacillus subtilis spores. J. Bacteriol. 2007, 189:1090-1098.
85. Johnstone K., et al. Zinc release and the sequence of biochemical events during triggering of Bacillus megaterium Km spore germination. Biochem. J. 1982, 208:407-411.
86. Li Y.F., et al. Role of a SpoVA protein in dipicolinic acid uptake into developing spores of Bacillus subtilis. J. Bacteriol. 2012, 194:1875-1884.
87. Setlow B., et al. Release of small molecules during germination of spores of Bacillus species. J. Bacteriol. 2008, 190:4759-4763.
88. Setlow B., et al. Properties of spores of Bacillus subtilis blocked at an intermediate stage of spore germination. J. Appl. Bacteriol. 2001, 183:4894-4899.
89. Cowan A.E., et al. 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. 2003, 100:4209-4214.
90. Kong L., et al. Monitoring the kinetics of uptake of a nucleic acid dye during the germination of single spores of Bacillus species. Anal. Chem. 2010, 82:8717-8724.
91. Ishikawa S., et al. Regulation and characterization of a newly deduced cell wall hydrolase gene (cwlJ) which affects germination of Bacillus subtilis spores. J. Bacteriol. 1998, 180:1375-1380.
92. Setlow B., et al. Characterization of the germination of Bacillus megaterium spores lacking enzymes that degrade the spore cortex. J. Appl. Microbiol. 2009, 107:318-328.
93. Christie G., et al. Mutational analysis of Bacillus megaterium QM B1551 cortex-lytic enzymes. J. Bacteriol. 2010, 192:5378-5389.
94. Moir A. How do spores germinate?. J. Appl. Microbiol. 2006, 101:526-530.
95. Reineke K. Mechanisms of Bacillus spore germination and inactivation during high pressure processing. Department of Food Biotechnology and Food Process Engineering 2012, 112-119. Technische Universität Berlin.