Advertisement

Food Engineering Reviews

, Volume 9, Issue 3, pp 122–142 | Cite as

A Quasi-chemical Model for Bacterial Spore Germination Kinetics by High Pressure

  • Christopher J. DoonaEmail author
  • Florence E. Feeherry
  • Kenneth Kustin
  • Haiqing Chen
  • Runze Huang
  • X. Philip Ye
  • Peter Setlow
Review Article

Abstract

High pressure processing (HPP) is an emerging non-thermal technology that is growing exponentially in use worldwide for the pasteurization of commercial foodstuffs. At combinations of elevated pressures and temperatures, HPP inactivates bacterial spores, but HPP has not yet been implemented commercially for food sterilization. Studies of the mechanisms of bacterial spore inactivation by HPP using primarily spores of Bacillus species have shown that spore germination precedes inactivation, with the release of dipicolinic acid from the spore core as the rate-determining step. Investigations probing spore resistance to and germination by HPP using Bacillus subtilis, a number of selected B. subtilis mutants, Bacillus amyloliquefaciens, and Clostridium difficile spores have compiled a wealth of detailed mechanistic information, while also accumulating abundant germination kinetics data that has not previously been analyzed by predictive models. Presently, we devise a “quasi-chemical” model for bacterial spore germination dynamics by HPP. This quasi-chemical germination model (QCGM) hypothesizes a three-step mechanism and derives a set of ordinary differential equations to model the observed germination dynamics. The results with this model are viewed in the context of historical studies of spore activation, germination, and inactivation, with an eye toward potentially integrating differential equation models for germination and inactivation into a single, comprehensive model for spore dynamics by HPP. With the increasing use of high hydrostatic pressure to investigate mechanisms of bacterial spore resistance and physiology, the QCGM results help promote the efficient control of bacterial spores, whether for the inactivation of Clostridium botulinum spores in low-acid foods or aerosolized Bacillus anthracis spores on textiles used in protective clothing, tents, or shelters.

Keywords

Spore germination and inactivation (B. subtilis, B. amyloliquefaciens, C. difficileHigh pressure processing Quasi-chemical predictive model SEM TEM 

Notes

Acknowledgements

The authors would like to thank Mr. Jay Jones (NSRDEC) for helpful discussions.

References

  1. 1.
    Anellis A, Grecz N, Berkowitz D (1965) Survival of Clostridium botulinum spores. Appl Microbiol 13(3):397–401Google Scholar
  2. 2.
    Anellis A, Koch RB (1962) Comparative resistance of strains of Clostridium botulinum to gamma rays. Appl Microbiol 10:326–330Google Scholar
  3. 3.
    Anellis A, Grecz N, Huber DA, Berkowitz D, Schneider MD, Simon M (1965) Radiation sterilization of bacon for military feeding. Appl Microbiol 13(1):37–42Google Scholar
  4. 4.
    Chambliss G, Vary JC eds (1978) Spores VII. Papers presented at the Seventh International Spore Conference, Madison, WI, 5–8 October 1977. American Society for Microbiology, Washington, pp ixGoogle Scholar
  5. 5.
    Doona CJ, Kustin K, Feeherry FE (2010) Case studies in novel food processing technologies: innovations in processing packaging, and predictive modeling. Woodhead Publishing, Oxford 529 ppCrossRefGoogle Scholar
  6. 6.
    Gould GW (1995) New methods of food preservation. Blackie Academic & Professional, GlasgowCrossRefGoogle Scholar
  7. 7.
    Siemer C, Toepfl S, Heinz V (2014) Inactivation of Bacillus subtilis spores by pulsed electric fields (PEF) in combination with thermal energy—I. Influence of process- and product parameters. Food Control 39:163–171CrossRefGoogle Scholar
  8. 8.
    Siemer C, Toepfl S, Heinz V (2014) Inactivation of Bacillus subtilis spores by pulsed electric fields (PEF) in combination with thermal energy II. Modeling thermal inactivation of B. subtilis spores during PEF processing in combination with thermal energy. Food Control 39:244–250CrossRefGoogle Scholar
  9. 9.
    Toepfl S, Siemer C, Saldaña-Navarro G, Heinz V (2014) Chapter 6—overview of pulsed electric fields processing for food. In: Sun D-W (ed) Emerging technologies for food processing, 2nd edn. Academic, San Diego, CA, pp. 93–114CrossRefGoogle Scholar
  10. 10.
    Diels AM, Michiels CW (2006) High-pressure homogenization as a non-thermal technique for the inactivation of microorganisms. Crit Rev Microbiol 32:201–216CrossRefGoogle Scholar
  11. 11.
    Georget E, Miller B, Aganovic K, Callanan M, Heinz V, Mathys A (2014a) Bacterial spore inactivation by ultra-high pressure homogenization. Innovative Food Science and Emerging Technology 26:116–123CrossRefGoogle Scholar
  12. 12.
    Georget E, Miller B, Callanan M, Heinz V, Mathys A (2014b) (ultra) high pressure homogenization for continuous high pressure sterilization of pumpable foods-a review. Frontiers in Nutrition 1:15CrossRefGoogle Scholar
  13. 13.
    Park SH, Balasubramaniam VM, Sastry SK, Lee J (2013) Pressure-ohmic-thermal sterilization: a feasible approach for the inactivation of Bacillus amyloliquefaciens and Geobacillus stearothermophilus spores. Innovative food science and emerging Technology 19, 115–123.Google Scholar
  14. 14.
    Balasubramaniam VM, Farkas D, Turek EJ (2008) Preserving foods through high-pressure processing. Food Technol 62(11):32–38Google Scholar
  15. 15.
    Doona CJ, Feeherry FE, Ross EW, Corradini M, Peleg M (2007) The quasi-chemical and Weibull distribution models of nonlinear inactivation kinetics of Escherichia coli ATCC 11229 by high pressure processing. In: Doona CJ, Feeherry (eds) High pressure processing of foods. IFT Press/Blackwell, Ames, IA, pp. 115–144CrossRefGoogle Scholar
  16. 16.
    Zhang HQ, Barbosa-Cánovas GV, Balasubramaniam VM, Dunne CP, Farkas DF, Yuan JTC (eds) (2011) Nonthermal processing technologies for food. IFT Press/Wiley-Blackwell, Ames, IAGoogle Scholar
  17. 17.
    Espar M (2015) Preserving fresh food longer without chemical—featured interview with Carole Tonello (Hiperbaric). FutureFood 2050 (available at http://futurefood2050.com/preserving-fresh-food-longer-without-chemicals/, accessed 9 September 2015)
  18. 18.
    Lingle R (2016) Surprising developments in HPP packaged foods. Packaging digest, Winter 2016, (available at http://www.packagingdigest.com/food-packaging/surprising-developments-hpp-packagedfoods-1511, accessed 13 Apr 2016)
  19. 19.
    Gassiot M, Masoliver P (2010) Commercial high pressure processing of ham and other sliced meat products at Esteban Espuña, SA. In: Doona CJ, Kustin K, Feeherry FE (eds) Case studies in novel food processing technologies: innovations in processing, packaging, and predictive modeling. Woodhead Publishing, Oxford, pp. 21–33CrossRefGoogle Scholar
  20. 20.
    Lingle R (2015) Unique chilled soups are bottled and high-pressure processed. Packaging Digest, Fall 2015 (available at http://www.packagingdigest.com/bottles/unique-chilled-soups-are-bottled-and-high-pressure-processed - accessed 3 May 2016)
  21. 21.
    Doona CJ, Feeherry FE, Ross EW, Kustin K (2012) Inactivation kinetics of Listeria monocytogenes by high-pressure processing: pressure and temperature variation. J Food Sci 77(8):M458–M465CrossRefGoogle Scholar
  22. 22.
    Doona CJ, Kustin K, Feeherry FE (2016) Mathematical models based on transition state theory for the microbial safety of foods by high pressure. In: Balasubramaniam VM, Barbosa-Cánovas GV, Lelieveld HLM (eds) High pressure processing of foods: principles, technology, and applications. Springer, NY, pp. 331–353CrossRefGoogle Scholar
  23. 23.
    US Food and Drug Administration (2012) Bad bug book—foodborne pathogenic microorganisms and natural toxins handbook. Listeria monocytogenes (available at http://www.fda.gov/downloads/Food/FoodborneIllnessContamiants/UCM297627.pdf, accessed 15 September 2015)
  24. 24.
    IIT-IFSH (2015) IFSH receives FDA acceptance of pressure enhanced sterilization process for commercial production of multicomponent shelf-stable foods. Food Safety Magazine, June/July 2015 (available at: http://www.foodsafetymagazine.com/news/ifsh-receives-fda-acceptance-of-pressure-enhanced-sterilization-process-for-commercial-production-of-multicomponent-shelf-stable-foods/)
  25. 25.
    Lau MH, Turek EJ (2007) Determination of quality differences in low-acid food sterilized by high pressure versus retorting. Ch 9. In: Doona CJ, Feeherry FE (eds) High pressure processing of food. IFT Press-Blackwell Publishing, Ames, pp. 195–219Google Scholar
  26. 26.
    Barbosa-Cánovas GV, Juliano P (2008) Food sterilization by combining high pressure and thermal energy. In: Gutierrez-López GF, Barbosa-Cánovas GV, Welti-Chanes J, Paradas-Arias E (eds) Food engineering: integrated approaches. Springer, NY, pp. 9–46CrossRefGoogle Scholar
  27. 27.
    Knoerzer K, Juliano P, Gladman S, Versteeg C, Fryer PJ (2007) A computational model for temperature and sterility distributions in a pilot-scale high-pressure high-temperature process. AICHE J 53:2996–3010CrossRefGoogle Scholar
  28. 28.
    Juliano P, Knoerzer K, Fryer PJ, Versteeg C (2009) Clostridium botulinum inactivation kinetics implemented in a computational model of a high-pressure sterilization process. Biotechnol Prog 25(1):163–175CrossRefGoogle Scholar
  29. 29.
    Bull MK, Olivier SA, van Diepenbeek RJ, Kormelink F, Chapman B (2009) Synergistic inactivation of spores of proteolytic Clostridium botulinum strains by high pressure and heat is strain- and product-dependent. Appl Environ Microbiol 75(2):434–445Google Scholar
  30. 30.
    Olivier SA, Smith R, Bull MK, Chapman B, Knoerzer K (2015) Apparatus for the simultaneous processing of mesophilic spores by heat-only and by high pressure and heat in a high pressure vessel to investigate synergistic spore inactivation. Innovative Food Science and Emerging Technologies 27:35–40CrossRefGoogle Scholar
  31. 31.
    Coleman WH, Chen D, Li Y-q, Cowan AE, Setlow P (2007) How moist heat kills spores of Bacillus subtilis. J Bacteriol 189:8458–8466CrossRefGoogle Scholar
  32. 32.
    Coleman WH, Zhang P, Li Y-q, Setlow P (2010) Mechanism of killing of spores of Bacillus cereus and Bacillus megaterium by wet heat. Lett Appl Microbiol 50:507–514CrossRefGoogle Scholar
  33. 33.
    Wang G, Zhang P, Setlow P, Li Y-q (2011) Kinetics of germination of wet-heat-treated individual spores of Bacillus species, monitored by Raman spectroscopy and differential interference contrast microscopy. Appl Environ Microbiol 77(10):3368–3379CrossRefGoogle Scholar
  34. 34.
    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 76:1796–1805CrossRefGoogle Scholar
  35. 35.
    Doona CJ, Feeherry FE, Setlow P, Malkin A, Leighton T (2014) “The PCS, D-FENS, and D-FEND ALL: Novel Chlorine Dioxide Decontamination Technologies for the Military.” Journal of Visualized Experiments 88, e4354 (available at http://www.jove.com/video/4354/the-portable-chemical-sterilizer-pcs-d-fens-d-fend-all-novel-chlorine, accessed 6 July 2015) JoVE Bioengineering).
  36. 36.
    Setlow P (2006) Spores of Bacillus subtilis: their resistance to radiation, heat and chemicals. J Appl Microbiol 101:514–525CrossRefGoogle Scholar
  37. 37.
    Setlow P (2007) Germination of spores of Bacillus subtilis by high pressure. In: Doona CJ, Feeherry (eds) High pressure processing of foods. IFT Press/Blackwell, Ames, IA, pp. 15–40CrossRefGoogle Scholar
  38. 38.
    Setlow P (2010) Bacterial spores. In: Hodges N, Hanlon G (eds) Industrial pharmaceutical microbiology, Supplement 10, Euromed Communications, Passfield, England, pp S10.1-S10.16Google Scholar
  39. 39.
    Setlow P, Johnson EA (2007) Spores and their significance. In: Doyle MP, Beuchat LR (eds) Food microbiology: fundamentals and frontiers, 3rd edn. ASM Press, Washington, pp. 35–47CrossRefGoogle Scholar
  40. 40.
    Levinson HL, Hyatt MT (1966) Sequence of events during Bacillus megaterium spore germination. J Bacteriol 91(5):1811–1818Google Scholar
  41. 41.
    Luu S, Cruz-Mora J, Setlow B, Feeherry FE, Doona CJ, Setlow P (2015) The effects of heat activation on bacillus spore germination with nutrients or under high pressure, with or without various germination proteins. Appl Environ Microbiol 81(8):2927–2938CrossRefGoogle Scholar
  42. 42.
    Vary JC, Halvorson HO (1965) Kinetics of germination of Bacillus spores. J Bacteriol 89(5):1340–1347Google Scholar
  43. 43.
    Halmann M, Keynan A (1962) Stages in germination of spores of Bacillus licheniformis. J Bacteriol 84:1187–1193Google Scholar
  44. 44.
    Yi X, Setlow P (2010) Studies of the commitment step in the germination of spores of Bacillus species. J Bacteriol 192(13):3424–3433CrossRefGoogle Scholar
  45. 45.
    Zhang P, Liang J, Yi X, Setlow P, Li Y-q (2014) Monitoring of commitment, blocking, and continuation of nutrient germination of individual Bacillus subtilis spores. J Bacteriol 196(13):2443–2454CrossRefGoogle Scholar
  46. 46.
    Keynan A, Evenchik Z, Halvorson HO, Hastings JW (1964) Activation of bacterial endospores. J Bacteriol 88:313–318Google Scholar
  47. 47.
    Hyatt MT, Levinson HS (1968) Water vapor, aqueous ethyl alcohol, and heat activation of Bacillus megaterium spore germination. J Bacteriol 95(6):2090–2101Google Scholar
  48. 48.
    Knorr D (1999) Curr Opin Biotechnol 10(5):485–491CrossRefGoogle Scholar
  49. 49.
    Raso J, Barbosa-Cánovas G (2003) Nonthermal preservation of foods using combined processing techniques. Crit Rev Food Sci Nutr 43(8):265–285CrossRefGoogle Scholar
  50. 50.
    Sale AJH, Gould GW, Hamilton WA (1970) Inactivation of bacterial spores by hydrostatic pressure. J Gen Microbiol 60(3):323–334CrossRefGoogle Scholar
  51. 51.
    Black EP, Koziol-Dube KK, Guan D, Wei J, Setlow B, Cortezzo DE, Hoover DG, Setlow P (2005) Factors influencing the germination of Bacillus subtilis spores via the activation of nutrient receptors by high pressure. Appl Environ Microbiol 71:5879–5887CrossRefGoogle Scholar
  52. 52.
    Black EP, Wei J, Atluri S, Cortezzo DE, Koziol-Dube K, Hoover DG, Setlow P (2007) Analysis of factors influencing the rate of germination of spores of Bacillus subtilis by very high pressure. J Appl Microbiol 102:65–76CrossRefGoogle Scholar
  53. 53.
    Doona CJ, Ghosh S, Feeherry FF, Ramirez-Peralta A, Huang Y, Chen H, Setlow P (2014) High pressure germination of Bacillus subtilis spores with alterations in levels and types of germination proteins. J Appl Microbiol 117:711–720CrossRefGoogle Scholar
  54. 54.
    Paidhungat M, Setlow B, Daniels WB, Hoover D, Papafragkou E, Setlow P (2002) Mechanisms of induction of germination of Bacillus subtilis spores by high pressure. Appl Environ Microbiol 68:3172–3175CrossRefGoogle Scholar
  55. 55.
    Reineke K, Mathys A, Heinz V, Knorr D (2013a) Mechanisms of endospore inactivation under high pressure. Trends Microbiol 21:296–304CrossRefGoogle Scholar
  56. 56.
    Wuytack EY, Boven S, Michiels CW (1998) Comparative study of pressure-induced germination of Bacillus subtilis spores at low and high pressures. Appl Environ Microbiol 64:3220–3224Google Scholar
  57. 57.
    Kong L, Doona CJ, Setlow P, Li Y-Q (2014) Monitoring rates and heterogeneity of high-pressure germination of Bacillus spores by phase-contrast microscopy of individual spores. Appl Environ Microbiol 80(1):345–353CrossRefGoogle Scholar
  58. 58.
    Kong L, Zhang P, Wang G, Yu J, Setlow P, Li Y-q (2011) Characterization of bacterial spore germination using phase-contrast and fluorescence microscopy, Raman spectroscopy, and optical tweezers. Nat Protoc 6(5):625–639CrossRefGoogle Scholar
  59. 59.
    Rode LJ, Foster J (1960) The action of surfactants on bacterial spores. Arch Mikrobiol 36:67–94CrossRefGoogle Scholar
  60. 60.
    Paidhungat M, Setlow B, Driks A, Setlow P (2000) Characterization of spores of Bacillus subtilis which lack dipicolinic acid. J Bacteriol 182:5505–5512CrossRefGoogle Scholar
  61. 61.
    Perez-Valdespino A, Li Y, Setlow B, Ghosh S, Pan D, Korza G, Feeherry FE, Doona CJ, Li Y-q, Hao B, Setlow P (2014) Properties and function of the SpoVAEa and SpoVAF proteins of Bacillus subtilis spores. J Bacteriol 196(11):2077–2088CrossRefGoogle Scholar
  62. 62.
    Doona CJ, Feeherry FE, Ross EW, Kustin K (2016) Chemical kinetics for the microbial safety of foods treated with high pressure processing or hurdles. Food Engineering Reviews 8(3):272–291CrossRefGoogle Scholar
  63. 63.
    Reineke K, Doehner I, Schlumbach K, Baier D, Mathys A, Knorr D (2012) The different pathways of spore germination and inactivation in dependence on pressure and temperature. Innovative Food Science and Emerging Technologies 13:31–41CrossRefGoogle Scholar
  64. 64.
    Wang G, Zhang P, Paredes-Sabja D, Green C, Setlow P, Sarker MR, Y-q L (2011) Analysis of the germination of individual Clostridium perfringens spores and its heterogeneity. J Appl Microbiol 111:1212–1223CrossRefGoogle Scholar
  65. 65.
    Dembek M, Stable RA, Witney AA, Wren BW, Fairweather NF (2013) Transcriptional analysis of temporal gene expression in germinating Clostridium difficile 630 endospores. PLoS One 15:e64011. doi: 10.1371/journal.pone.0064011 CrossRefGoogle Scholar
  66. 66.
    Wang S, Shen A, Setlow P, Li Y-q (2015) Characterization of the dynamic germination of individual Clostridium difficile spores using Raman spectroscopy and differential interference contrast microscopy. J Bacteriol 197:2361–2373CrossRefGoogle Scholar
  67. 67.
    Doona CJ, Feeherry FE, Setlow B, Wang S, Li W, Nichols F, Talukdar P, Sarker M, Li Y-q, Shen A, Setlow P (2016) Effects of high pressure treatment on spores of Clostridium species. Appl Environ Microbiol 82(17):5287–5297 (featured in AEM spotlight)CrossRefGoogle Scholar
  68. 68.
    Ghosh S, Setlow P (2009) Isolation and characterization of superdormant spores of Bacillus species. J Bacteriol 191(6):1787–1797CrossRefGoogle Scholar
  69. 69.
    Frazier WC, Westhoff DC (1978) Food microbiology, 3rd edn. McGraw-Hill Book company, New York, NY, p. 95Google Scholar
  70. 70.
    Reineke K, Ellinger N, Berger D, Baier D, Mathys A, Setlow P, Knorr D (2013) Structural analysis of high pressure treated Bacillus subtilis spores. Innovative Science and Emerging Technologies 17:43–53CrossRefGoogle Scholar
  71. 71.
    Reineke K, Schlumbach K, Baier D, Mathys A, Knorr D (2013b) 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(1):55–63CrossRefGoogle Scholar
  72. 72.
    Sevenich R, Bark F, Crews C, Anderson W, Riddellova K, Hradecky J, Moravcova E, Reineke K, Knorr D (2013) Effect of high pressure thermal sterilization on the formation of food processing contaminants. Innovative Food Science and Emerging Technologies 20:42–50CrossRefGoogle Scholar
  73. 73.
    Sevenich R, Kleinstueck E, Crews C, Anderson W, Pye C, Riddellova K, Hradecky J, Moravcova E, Reineke K, Knorr D (2013) High-pressure thermal sterilization: food safety and food quality of baby food purée. J Food Sci 79(2):M230–M238CrossRefGoogle Scholar
  74. 74.
    Woese RC, Vary JC, Halvorson HO (1968) A kinetic model for bacterial spore germination. Proc Natl Acad Sci 59(3):869–875CrossRefGoogle Scholar
  75. 75.
    Setlow P, Liu J, Faeder J (2012) Heterogeneity in bacterial spore populations. In: Abel-Santos E (ed) Bacterial spores: current research and applications. Caister Academic Press, Norfolk, pp. 199–215Google Scholar
  76. 76.
    McCormick NG (1965) Kinetics of spore germination. J Bacteriol 89(5):1180–1185Google Scholar
  77. 77.
    Peleg M, Corradini MG, Normand MD (2012) On quantifying nonthermal effects on the lethality of pressure-assisted heat preservation processes. J Food Sci 71(1):R47–R56CrossRefGoogle Scholar
  78. 78.
    Peleg M, Normand MD (2013) Modeling of fungal and bacterial spore germination under static and dynamic conditions. Appl Environ Microbiol 79(21):6765–6775CrossRefGoogle Scholar
  79. 79.
    Margosch D, Ehrmann MA, Gänzle MG, Vogel RF (2004) Comparison of pressure and heat resistance of Clostridium botulinum and other endospores in mashed carrots. J Food Prot 67:2530–2537CrossRefGoogle Scholar
  80. 80.
    Adams CM, Eckenroth BE, Putnam EE, Doublie S, Shen A (2013). Structural and functional analysis of the CspB protease required for Clostridium spore germination. PLoS Pathog 9:e1003165. doi:  10.1371/journal.ppat.1003165.
  81. 81.
    Butzin XY, Troiano AJ, Coleman WH, Griffiths KK, Doona CJ, Feeherry FE, Wang G, Li Y-q, Setlow P (2012) Analysis of the effects of a gerP mutation on the germination of spores of Bacillus subtilis. J Bacteriol 194(21):5749–5758Google Scholar
  82. 82.
    Huang S-s, Chen D, Pelczar PL, Vepachedu VR, Setlow P, Li Y-Q (2007) Levels of Ca2+-dipicolinic acid in individual Bacillus spores determined using microfluidic Raman tweezers. J Bacteriol 189:4681–4687CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2017

Authors and Affiliations

  • Christopher J. Doona
    • 1
    Email author
  • Florence E. Feeherry
    • 1
  • Kenneth Kustin
    • 2
  • Haiqing Chen
    • 3
  • Runze Huang
    • 3
  • X. Philip Ye
    • 4
  • Peter Setlow
    • 5
  1. 1.US Army Natick Soldier RD&E CenterNatickUSA
  2. 2.Department of Chemistry, Emeritus, MS 015Brandeis UniversityWalthamUSA
  3. 3.Department of Animal and Food SciencesUniversity of DelawareNewarkUSA
  4. 4.Department of Biosystems Engineering and Soil ScienceUniversity of TennesseeKnoxvilleUSA
  5. 5.Department of Molecular Biology and BiophysicsUniversity of Connecticut Health CenterFarmingtonUSA

Personalised recommendations