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Abstract

Spore-forming bacteria are ubiquitous in nature. The resistance properties of bacterial spores lie at the heart of their widespread occurrence in food ingredients and foods. The efficacy of inactivation by food-processing conditions is largely determined by the characteristics of the different types of spores, whereas food composition and storage conditions determine the eventual germination and outgrowth of surviving spores. Here, we review the current knowledge on variation in spore resistance, in germination, and in the outgrowth capacity of spores relevant to foods. This includes novel findings on key parameters in spore survival and outgrowth obtained by gene-trait matching approaches using genome-sequenced spp. food isolates, which represent notorious food spoilage and pathogenic species. Additionally, the impact of strain diversity on heat inactivation of spores and the variability therein is discussed. Knowledge and quantification of factors that influence variability can be applied to improve predictive models, ultimately supporting effective control of spore-forming bacteria in foods.

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2016-02-28
2024-04-18
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Literature Cited

  1. Abbas AA, Planchon S, Jobin M, Schmitt P. 2014. Absence of oxygen affects the capacity to sporulate and the spore properties of Bacillus cereus. Food Microbiol. 42:122–31 [Google Scholar]
  2. Abee T, Groot MN, Tempelaars M, Zwietering M, Moezelaar R, van der Voort M. 2011. Germination and outgrowth of spores of Bacillus cereus group members: diversity and role of germinant receptors. Food Microbiol. 28:199–208 [Google Scholar]
  3. Abhyankar W, Pandey R, Ter Beek A, Brul S, de Koning LJ, de Koster CG. 2015. Reinforcement of Bacillus subtilis spores by cross-linking of outer coat proteins during maturation. Food Microbiol. 45:Pt. A54–62 [Google Scholar]
  4. Afchain AL, Carlin F, Nguyen-The C, Albert I. 2008. Improving quantitative exposure assessment by considering genetic diversity of Bacillus cereus in cooked, pasteurized and chilled foods. Int. J. Food Microbiol. 128:165–73 [Google Scholar]
  5. Aguirre JS, de Fernando GG, Hierro E, Hospital XF, Ordóñez JA, Fernández M. 2015. Estimation of the growth kinetic parameters of Bacillus cereus spores as affected by pulsed light treatment. Int. J. Food Microbiol. 202:20–26 [Google Scholar]
  6. Ahn J, Balasubramaniam VM, Yousef AE. 2007. Inactivation kinetics of selected aerobic and anaerobic bacterial spores by pressure-assisted thermal processing. Int. J. Food Microbiol. 113:321–29 [Google Scholar]
  7. Albertsen M, Hugenholtz P, Skarshewski A, Nielsen KL, Tyson GW, Nielsen PH. 2013. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat. Biotechnol. 31:6533–38 [Google Scholar]
  8. Al-Hinai MA, Jones SW, Papoutsakis ET. 2015. The Clostridium sporulation programs: diversity and preservation of endospore differentiation. Microbiol. Mol. Biol. Rev. 79:119–37 [Google Scholar]
  9. Anderson Borge GI, Skeie M, Sørhaug T, Langsrud T, Granum PE. 2001. Growth and toxin profiles of Bacillus cereus isolated from different food sources. Int. J. Food Microbiol. 69:3237–46 [Google Scholar]
  10. Anderson NM, Larkin JW, Cole MB, Skinner GE, Whiting RC. et al. 2011. Food safety objective approach for controlling Clostridium botulinum growth and toxin production in commercially sterile foods. J. Food Prot. 74:111956–89 [Google Scholar]
  11. Andersson A, Ronner U, Granum PE. 1995. What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens?. Int. J. Food Microbiol. 28:2145–55 [Google Scholar]
  12. André S, Zuber F, Remize F. 2013. Thermophilic spore-forming bacteria isolated from spoiled canned food and their heat resistance. Results of a French ten-year survey. Int. J. Food Microbiol. 165:2134–43 [Google Scholar]
  13. Augustin JC. 2011. Challenges in risk assessment and predictive microbiology of foodborne spore-forming bacteria. Food Microbiol. 28:2209–13 [Google Scholar]
  14. Balasubramaniam VM, Martínez-Monteagudo SI, Gupta R. 2015. Principles and application of high pressure–based technologies in the food industry. Annu. Rev. Food Sci. Technol. 6:435–62 [Google Scholar]
  15. Bayjanov JR, Molenaar D, Tzeneva V, Siezen RJ, van Hijum SA. 2012. PhenoLink—a web-tool for linking phenotype to ∼omics data for bacteria: application to gene-trait matching for Lactobacillus plantarum strains. BMC Genomics 13:170 [Google Scholar]
  16. Berendsen EM, Krawczyk AO, Klaus V, de Jong A, Boekhorst J. et al. 2015a. Spores of Bacillus thermoamylovorans with very high heat resistances germinate poorly in rich media despite the presence of ger clusters, but efficiently upon non-nutrient Ca-DPA exposure. Appl. Environ. Microbiol. 81:7791–801 [Google Scholar]
  17. Berendsen EM, Zwietering MH, Kuipers OP, Wells-Bennik MHJ. 2015b. Two distinct groups within the Bacillus subtilis group display significantly different spore heat resistance properties. Food Microbiol. 45:Pt. A18–25 [Google Scholar]
  18. Billon CM, McKirgan CJ, McClure PJ, Adair C. 1997. The effect of temperature on the germination of single spores of Clostridium botulinum 62A. J. Appl. Microbiol. 82:148–56 [Google Scholar]
  19. Brunt J, Plowman J, Gaskin DJ, Itchner M, Carter AT, Peck MW. 2014. Functional characterisation of germinant receptors in Clostridium botulinum and Clostridium sporogenes presents novel insights into spore germination systems. PLOS Pathog. 10:9e1004382 [Google Scholar]
  20. Burgess SA, Lindsay D, Flint SH. 2010. Thermophilic bacilli and their importance in dairy processing. Int. J. Food Microbiol. 144:2215–25 [Google Scholar]
  21. Byrer DE, Rainey FA, Wiegel J. 2000. Novel strains of Moorella thermoacetica form unusually heat-resistant spores. Arch. Microbiol. 174:334–39 [Google Scholar]
  22. Campos SS, Ibarra-Rodriguez JR, Barajas-Ornelas RC, Ramírez-Guadiana FH, Obregón-Herrera A. et al. 2014. Interaction of apurinic/apyrimidinic endonucleases Nfo and ExoA with the DNA integrity scanning protein DisA in the processing of oxidative DNA damage during Bacillus subtilis spore outgrowth. J. Bacteriol. 196:3568–78 [Google Scholar]
  23. Carlin F, Albagnac C, Rida A, Guinebretière MH, Couvert O, Nguyen-The C. 2013. Variation of cardinal growth parameters and growth limits according to phylogenetic affiliation in the Bacillus cereus group. Consequences for risk assessment. Food Microbiol. 33:169–76 [Google Scholar]
  24. Carlin F, Fricker M, Pielaat A, Heisterkamp S, Shaheen R. et al. 2006. Emetic toxin-producing strains of Bacillus cereus show distinct characteristics within the Bacillus cereus group. Int. J. Food Microbiol. 109:132–38 [Google Scholar]
  25. Carlin F. 2011. Origin of bacterial spores contaminating foods. Food Microbiol. 28:2177–82 [Google Scholar]
  26. Carter AT, Peck MW. 2015. Genomes, neurotoxins and biology of Clostridium botulinum group I and group II. Res. Microbiol. 166:4303–17 [Google Scholar]
  27. Cazemier AE, Wagenaars SFM, Ter Steeg PF. 2001. Effect of sporulation and recovery medium on the heat resistance and amount of injury of spores from spoilage bacilli. J. Appl. Microbiol. 90:761–70 [Google Scholar]
  28. Chang SS, Kang DH. 2004. Alicyclobacillus spp. in the fruit juice industry: History, characteristics, and current isolation/detection procedures. Crit. Rev. Microbiol. 30:255–74 [Google Scholar]
  29. Checinska A, Paszczynski A, Burbank M. 2015. Bacillus and other spore-forming genera: variations in responses and mechanisms for survival. Annu. Rev. Food Sci. Technol. 6:351–69 [Google Scholar]
  30. Chen D, Huang SS, Li YQ. 2006. Real-time detection of kinetic germination and heterogeneity of single Bacillus spores by laser tweezers Raman spectroscopy. Anal. Chem. 78:196936–41 [Google Scholar]
  31. Chondrogianni N, Petropoulos I, Grimm S, Georgila K, Catalgol B. et al. 2014. Protein damage, repair and proteolysis. Mol. Aspects Med. 35:1–71 [Google Scholar]
  32. Chu S, Hawes JW, Lorigan GA. 2009. Solid-state NMR spectroscopic studies on the interaction of sorbic acid with phospholipid membranes at different pH levels. Magn. Reson. Chem. 47:651–57 [Google Scholar]
  33. Coleman WH, Chen D, Li Y-Q, Cowan AE, Setlow P. 2007. How moist heat kills spores of Bacillus subtilis. J. Bacteriol. 189:8458–66 [Google Scholar]
  34. 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. 50:507–14 [Google Scholar]
  35. Cronin UP, Wilkinson MG. 2010. The potential of flow cytometry in the study of Bacillus cereus. J. Appl. Microbiol. 108:11–16 [Google Scholar]
  36. Daelman J, Membré JM, Jacxsens L, Vermeulen A, Devlieghere F, Uyttendaele M. 2013. A quantitative microbiological exposure assessment model for Bacillus cereus in REPFEDs. Int. J. Food Microbiol. 166:3433–49 [Google Scholar]
  37. Daniels JK, Caldwell TP, Christensen KA, Chumanov G. 2006. Monitoring the kinetics of Bacillus subtilis endospore germination via surface-enhanced Raman scattering spectroscopy. Anal. Chem. 78:51724–29 [Google Scholar]
  38. de Jong IG, Beilharz K, Kuipers OP, Veening JW. 2011. Live cell imaging of Bacillus subtilis and Streptococcus pneumoniae using automated time-lapse microscopy. J. Vis. Exp. 53:3145 [Google Scholar]
  39. de Jong IG, Veening JW, Kuipers OP. 2010. Heterochronic phosphorelay gene expression as a source of heterogeneity in Bacillus subtilis spore formation. J. Bacteriol. 192:82053–67 [Google Scholar]
  40. den Besten HMW, van Melis CCJ, Sanders JW, Nierop Groot MN, Abee T. 2012. Impact of sorbic acid on germination and outgrowth heterogeneity of Bacillus cereus ATCC 14579 spores. Appl. Environ. Microbiol. 78:238477–80 [Google Scholar]
  41. Doyle CJ, Gleeson D, Jordan K, Beresford TP, Ross RP. et al. 2015. Anaerobic sporeformers and their significance with respect to milk and dairy products. Int. J. Food Microbiol. 197:77–87 [Google Scholar]
  42. Ducret A, Maisonneuve E, Notareschi P, Grossi A, Mignot T, Dukan S. 2009. A microscope automated fluidic system to study bacterial processes in real time. PLOS ONE 4:9e7282 [Google Scholar]
  43. Durand L, Planchon S, Guinebretiere MH, Carlin F, Remize F. 2015. Genotypic and phenotypic characterization of foodborne Geobacillus stearothermophilus. Food Microbiol. 45:Pt. A103–10 [Google Scholar]
  44. EFSA (Eur. Food Saf. Auth.) 2005. Opinion of the scientific panel on biological hazards on Bacillus cereus and other Bacillus spp in foodstuffs. EFSA J. 175:1–48 [Google Scholar]
  45. 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. 22:180–86 [Google Scholar]
  46. Eijlander RT, de Jong A, Krawczyk AO, Holsappel S, Kuipers OP. 2014. SporeWeb: an interactive journey through the complete sporulation cycle of Bacillus subtilis. Nucleic Acids Res. 42:D685–91 [Google Scholar]
  47. Eijlander RT, Kuipers OP. 2013. Live-cell imaging tool optimization to study gene expression levels and dynamics in single cells of Bacillus cereus. Appl. Environ. Microbiol. 79:185643–51 [Google Scholar]
  48. Evanoff DD Jr, Heckel J, Caldwell TP, Christensen KA, Chumanov G. 2006. Monitoring DPA release from a single germinating Bacillus subtilis endospore via surface-enhanced Raman scattering microscopy. J. Am. Chem. Soc. 128:3912618–19 [Google Scholar]
  49. Galperin MY, Mekhedov SL, Puigbo P, Smirnov S, Wolf YI, Rigden DJ. 2012. Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environ. Microbiol. 14:112870–90 [Google Scholar]
  50. Gerhardt P, Marquis RE. 1989. Spore thermoresistance mechanisms. Regulation of Prokaryotic Development I Smith, RA Slepecky, P Setlow 17–63 Washington, DC: Am. Soc. Microbiol. [Google Scholar]
  51. Ghosh S, Korza G, Maciejewski M, Setlow P. 2015. Analysis of metabolism in dormant spores of Bacillus species by 31P nuclear magnetic resonance analysis of low-molecular-weight compounds. J. Bacteriol. 197:992–1001 [Google Scholar]
  52. Ghosh S, Ramirez-Peralta A, Gaidamakova E, Zhang P, Li YQ. et al. 2011. Effects of Mn levels on resistance of Bacillus megaterium spores to heat, radiation and hydrogen peroxide. J. Appl. Microbiol. 111:663–70 [Google Scholar]
  53. Ghosh S, Scotland M, Setlow P. 2012. Levels of germination proteins in dormant and superdormant spores of Bacillus subtilis. J. Bacteriol. 194:92221–27 [Google Scholar]
  54. Ghosh S, Setlow P. 2009. Isolation and characterization of superdormant spores of Bacillus species. J. Bacteriol. 191:1787–97 [Google Scholar]
  55. Ghosh S, Zhang P, Li YQ, Setlow P. 2009. Superdormant spores of Bacillus species have elevated wet-heat resistance and temperature requirements for heat activation. J. Bacteriol. 191:185584–91 [Google Scholar]
  56. Gioia J, Yerrapragada S, Qin X, Jiang H, Igboeli OC. et al. 2007. Paradoxical DNA repair and peroxide resistance gene conservation in Bacillus pumilus SAFR-032. PLOS ONE 2:9e928 [Google Scholar]
  57. Gould GW. 1996. Methods for preservation and extension of shelf life. Int. J. Food Microbiol. 33:151–64 [Google Scholar]
  58. Granger AC, Gaidamakova EK, Matrosova VY, Daly MJ, Setlow P. 2011. Effects of Mn and Fe levels on Bacillus subtilis spore resistance and effects of Mn2+, other divalent cations, orthophosphate, and dipicolinic acid on protein resistance to ionizing radiation. Appl. Environ. Microbiol. 77:32–40 [Google Scholar]
  59. Griffiths KK, Setlow P. 2009. Effects of modification of membrane lipid composition on Bacillus subtilis sporulation and spore properties. J. Appl. Microbiol. 106:2064–78 [Google Scholar]
  60. Guinebretière M-H, Thompson FL, Sorokin A, Normand P, Dawyndt P. et al. 2008. Ecological diversification in the Bacillus cereus group. Environ. Microbiol. 10:4851–65 [Google Scholar]
  61. Gut IM, Blanke SR, van der Donk WA. 2011. Mechanism of inhibition of Bacillus anthracis spore outgrowth by the lantibiotic nisin. ACS Chem. Biol. 6:744–52 [Google Scholar]
  62. Henriques AO, Moran CP Jr. 2007. Structure, assembly, and function of the spore surface layers. Annu. Rev. Microbiol. 61:555–88 [Google Scholar]
  63. Heyndrickx M. 2011. The importance of endospore-forming bacteria originating from soil for contamination of industrial food processing. Appl. Environ. Soil Sci. 2011:11 [Google Scholar]
  64. Higgins D, Dworkin J. 2012. Recent progress in Bacillus subtilis sporulation. FEMS Microbiol. Rev. 36:1131–48 [Google Scholar]
  65. Hilbert DW, Piggot PJ. 2004. Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiol. Mol. Biol. Rev. 68:234–62 [Google Scholar]
  66. Ivy RA, Ranieri ML, Martin NH, den Bakker HC, Xavier BM. et al. 2012. Identification and characterization of psychrotolerant sporeformers associated with fluid milk production and processing. Appl. Environ. Microbiol. 78:1853–64 [Google Scholar]
  67. Kalinowski RM, Tompkin RB. 1999. Psychrotrophic clostridia causing spoilage in cooked meat and poultry products. J. Food Prot. 62:7766–72 [Google Scholar]
  68. Kong L, Zhang P, Setlow P, Li YQ. 2010. Characterization of bacterial spore germination using integrated phase contrast microscopy, Raman spectroscopy, and optical tweezers. Anal. Chem. 82:93840–47 [Google Scholar]
  69. Kong L, Zhang P, Wang G, Yu J, Setlow P, Li YQ. 2011. Characterization of bacterial spore germination using phase-contrast and fluorescence microscopy, Raman spectroscopy and optical tweezers. Nat. Protoc. 6:5625–39 [Google Scholar]
  70. Kort R, O'Brien AC, van Stokkum IHM, Oomes SJCM, Crielaard W. et al. 2005. Assessment of heat resistance of bacterial spores from food product isolates by fluorescence monitoring of dipicolinic acid release. Appl. Environ. Microbiol. 71:3556–64 [Google Scholar]
  71. Leggett MJ, McDonnell G, Denyer SP, Setlow P, Maillard JY. 2012. Bacterial spore structures and their protective role in biocide resistance. J. Appl. Microbiol. 113:485–98 [Google Scholar]
  72. Leguerinel I, Couvert O, Mafart P. 2000. Relationship between the apparent heat resistance of Bacillus cereus spores and the pH and NaCl concentration of the recovery medium. Int. J. Food Microbiol. 55:223–27 [Google Scholar]
  73. Lenhart JS, Schroeder JW, Walsh BW, Simmons LA. 2012. DNA repair and genome maintenance in Bacillus subtilis. Microbiol. Mol. Biol. Rev. 76:3530–64 [Google Scholar]
  74. Lenz CA, Vogel RF. 2015. Differential effects of sporulation temperature on the high pressure resistance of Clostridium botulinum type E spores and the interconnection with sporulation medium cation contents. Food Microbiol. 46:434–42 [Google Scholar]
  75. 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 [Google Scholar]
  76. Lima LJR, Kamphuis HJ, Nout MJR, Zwietering MH. 2011. Microbiota of cocoa powder with particular reference to aerobic thermoresistant sporeformers. Food Microbiol. 28:573–82 [Google Scholar]
  77. Logan NA. 2012. Bacillus and relatives in foodborne illness. J. Appl. Microbiol. 112:417–29 [Google Scholar]
  78. Løvdal IS, Hovda MB, Granum PE, Rosnes JT. 2011. Promoting Bacillus cereus spore germination for subsequent inactivation by mild heat treatment. J. Food Prot. 74:2079–89 [Google Scholar]
  79. Luu-Thi H, Khadka DB, Michiels CW. 2014. Thermal inactivation parameters of spores from different phylogenetic groups of Bacillus cereus. Int. J. Food Microbiol. 189:183–88 [Google Scholar]
  80. Mafart P. 2000. Taking injuries of surviving bacteria into account for optimising heat treatments. Int. J. Food Microbiol. 55:175–79 [Google Scholar]
  81. Mafart P, Leguérinel I, Couvert O, Coroller L. 2010. Quantification of spore resistance for assessment and optimization of heating processes: a never-ending story. Food Microbiol. 27:568–72 [Google Scholar]
  82. Margosch D, Ehrmann MA, Buckow R, Heinz V, Vogel RF, Gänzle MG. 2006. High-pressure-mediated survival of Clostridium botulinum and Bacillus amyloliquefaciens endospores at high temperature. Appl. Environ. Microbiol. 72:3476–81 [Google Scholar]
  83. Markland SM, Farkas DF, Kniel KE, Hoover DG. 2013. Pathogenic psychrotolerant sporeformers: an emerging challenge for low-temperature storage of minimally processed foods. Foodborne Pathog. Dis. 10:413–19 [Google Scholar]
  84. McKenney PT, Driks A, Eichenberger P. 2013. The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat. Rev. Microbiol. 11:33–44 [Google Scholar]
  85. Melly E, Genest PC, Gilmore ME, Little S, Popham DL. et al. 2002. Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. J. Appl. Microbiol. 92:1105–15 [Google Scholar]
  86. Melly E, Setlow P. 2001. Heat shock proteins do not influence wet heat resistance of Bacillus subtilis spores. J. Bacteriol. 183:779–84 [Google Scholar]
  87. Membré JM, Amézquita A, Bassett J, Giavedoni P, Blackburn CdeW, Gorris LGM. 2006. A probabilistic modeling approach in thermal inactivation: estimation of postprocess Bacillus cereus spore prevalence and concentration. J. Food Prot. 69:1118–29 [Google Scholar]
  88. Membré JM, Kan-King-Yu D, Blackburn CdeW. 2008. Use of sensitivity analysis to aid interpretation of a probabilistic Bacillus cereus spore lag time model applied to heat-treated chilled foods (REPFEDs). Int. J. Food Microbiol. 128:128–33 [Google Scholar]
  89. Mols M, Abee T. 2011. Bacillus cereus responses to acid stress. Environ. Microbiol. 13:2835–43 [Google Scholar]
  90. Moschonas G, Bolton DJ, McDowell DA, Sheridan JJ. 2011. Diversity of culturable psychrophilic and psychrotrophic anaerobic bacteria isolated from beef abattoirs and their environments. Appl. Environ. Microbiol. 77:134280–84 [Google Scholar]
  91. Movahedi S, Waites W. 2000. A two-dimensional protein gel electrophoresis study of the heat stress response of Bacillus subtilis cells during sporulation. J. Bacteriol. 182:4758–63 [Google Scholar]
  92. Müller S, Nebe-von-Caron G. 2010. Functional single-cell analyses: flow cytometry and cell sorting of microbial populations and communities. FEMS Microbiol. Rev. 34:554–87 [Google Scholar]
  93. Nguyen Thi Minh H, 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. Microbiol. Biotechnol. 90:1409–17 [Google Scholar]
  94. Nicholson WL. 2002. Roles of Bacillus endospores in the environment. Cell. Mol. Life Sci. 59:410–16 [Google Scholar]
  95. 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. 64:548–72 [Google Scholar]
  96. Ochman H, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304 [Google Scholar]
  97. Olguín-Araneda V, Banawas S, Sarker MR, Paredes-Sabja D. 2015. Recent advances in germination of Clostridium spores. Res. Microbiol. 166:236–43 [Google Scholar]
  98. Oomes SJCM, Brul S. 2004. The effect of metal ions commonly present in food on gene expression of sporulating Bacillus subtilis cells in relation to spore wet heat resistance. Innov. Food Sci. Emerg. Technol. 5:307–16 [Google Scholar]
  99. Oomes SJCM, van Zuijlen AC, Hehenkamp JO, Witsenboer H, van der Vossen JM, Brul S. 2007. The characterisation of Bacillus spores occurring in the manufacturing of (low acid) canned products. Int. J. Food Microbiol. 120:1–285–94 [Google Scholar]
  100. Orsburn B, Melville SB, Popham DL. 2008. Factors contributing to heat resistance of Clostridium perfringens endospores. Appl. Environ. Microbiol. 74:113328–35 [Google Scholar]
  101. Pandey R, Ter Beek A, Vischer NOE, Smelt JPPM, Brul S, Manders EMM. 2013. Live cell imaging of germination and outgrowth of individual Bacillus subtilis spores; the effect of heat stress quantitatively analyzed with SporeTracker. PLOS ONE 8:3e58972 [Google Scholar]
  102. Paredes CJ, Alsaker KV, Papoutsakis ET. 2005. A comparative genomic view of clostridial sporulation and physiology. Nat. Rev. Microbiol. 3:12969–78 [Google Scholar]
  103. Paredes-Sabja D, Shen A, Sorg JA. 2014. Clostridium difficile spore biology: sporulation, germination, and spore structural proteins. Trends Microbiol. 22:406–16 [Google Scholar]
  104. Pasha I, Saeed F, Sultan MT, Khan MR, Rohi M. 2014. Recent developments in minimal processing: a tool to retain nutritional quality of food. Crit. Rev. Food Sci. Nutr. 54:3340–51 [Google Scholar]
  105. Peck MW, Stringer SC, Carter AT. 2011. Clostridium botulinum in the post-genomic era. Food Microbiol. 28:183–91 [Google Scholar]
  106. Peng L, Chen D, Setlow P, Li YQ. 2009. Elastic and inelastic light scattering from single bacterial spores in an optical trap allows the monitoring of spore germination dynamics. Anal. Chem. 81:104035–42 [Google Scholar]
  107. Pielaat A, Fricker M, Nauta MJ, van Leusden FM. 2005. Biodiversity in Bacillus cereus RIVM Rep. 250912004/2005, Natl. Inst. Public Health Environ. Bilthoven, The Netherlands
  108. Popham DL. 2002. Specialized peptidoglycan of the bacterial endospore: the inner wall of the lockbox. Cell. Mol. Life Sci. 59:426–33 [Google Scholar]
  109. Postollec F, Mathot AG, Bernard M, Divanac'h ML, Pavan S, Sohier D. 2012. Tracking spore-forming bacteria in food: from natural biodiversity to selection by processes. Int. J. Food Microbiol. 158:1–8 [Google Scholar]
  110. Reineke K, Mathys A, Heinz V, Knorr D. 2013. Mechanisms of endospore inactivation under high pressure. Trends Microbiol. 21:296–304 [Google Scholar]
  111. Samapundo S, Devlieghere F, Xhaferi R, Heyndrickx M. 2014a. Incidence, diversity and characteristics of spores of psychrotolerant spore formers in various REPFEDS produced in Belgium. Food Microbiol. 44:288–95 [Google Scholar]
  112. Samapundo S, Heyndrickx M, Xhaferi R, de Baenst I, Devlieghere F. 2014b. The combined effect of pasteurization intensity, water activity, pH and incubation temperature on the survival and outgrowth of spores of Bacillus cereus and Bacillus pumilus in artificial media and food products. Int. J. Food Microbiol. 181:10–18 [Google Scholar]
  113. Sanchez-Salas J-L, Setlow B, Zhang P, Li Y-Q, Setlow P. 2011. Maturation of released spores is necessary for acquisition of full spore heat resistance during Bacillus subtilis sporulation. Appl. Environ. Microbiol. 77:196746–54 [Google Scholar]
  114. Sarker MR, Akhtar S, Torres JA, Paredes-Sabja D. 2015. High hydrostatic pressure-induced inactivation of bacterial spores. Crit. Rev. Microbiol. 41:18–26 [Google Scholar]
  115. Scheldeman P, Goossens K, Rodriguez-Diaz M, Pil A, Goris J. et al. 2004. Paenibacillus lactis sp. nov., isolated from raw and heat-treated milk. Int. J. Syst. Evol. Microbiol. 54:3885–91 [Google Scholar]
  116. Scheldeman P, Herman L, Foster S, Heyndrickx M. 2006. Bacillus sporothermodurans and other highly heat-resistant spore formers in milk. J. Appl. Microbiol. 101:542–55 [Google Scholar]
  117. Sedlak M, Vinter V, Adamec J, Vohradsky J, Voburka Z, Chaloupka J. 1993. Heat shock applied early in sporulation affects heat resistance of Bacillus megaterium spores. J. Bacteriol. 175:8049–52 [Google Scholar]
  118. Setlow B, Parish S, Zhang P, Li YQ, Neely WC, 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. 116:4805–14 [Google Scholar]
  119. Setlow P. 2003. Spore germination. Curr. Opin. Microbiol. 6:550–56 [Google Scholar]
  120. Setlow P. 2006. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 101:514–25 [Google Scholar]
  121. Setlow P. 2013. Summer meeting 2013—when the sleepers wake: the germination of spores of Bacillus species. J. Appl. Microbiol. 115:1251–68 [Google Scholar]
  122. Setlow P. 2014. Germination of spores of Bacillus species: what we know and do not know. J. Bacteriol. 196:1297–305 [Google Scholar]
  123. Shah IM, Laaberki M-H, Popham DL, Dworkin J. 2008. A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135:3486–96 [Google Scholar]
  124. Shearer AE, Mazzotta AS, Chuyate R, Gombas DE. 2002. Heat resistance of juice spoilage microorganisms. J. Food Prot. 65:81271–75 [Google Scholar]
  125. Silva FV, Gibbs P. 2004. Target selection in designing pasteurization processes for shelf-stable high-acid fruit products. Crit. Rev. Food Sci. Nutr. 44:5353–60 [Google Scholar]
  126. Sinai L, Rosenberg A, Smith Y, Segev E, Ben-Yehuda S. 2015. The molecular timeline of a reviving bacterial spore. Mol. Cell 57:4695–707 [Google Scholar]
  127. Smelt JPPM, Bos AP, Kort R, Brul S. 2008. Modelling the effect of sub(lethal) heat treatment of Bacillus subtilis spores on germination rate and outgrowth to exponentially growing vegetative cells. Int. J. Food Microbiol. 128:34–40 [Google Scholar]
  128. Stecchini ML, Del Torre M, Polese P. 2013. Survival strategies of Bacillus spores in food. Indian J. Exp. Biol. 51:905–9 [Google Scholar]
  129. Steyn CE, Cameron M, Witthuhn RC. 2011. Occurrence of Alicyclobacillus in the fruit processing environment—a review. Int. J. Food Microbiol. 147:1–11 [Google Scholar]
  130. Stringer SC, Webb MD, George SM, Pin C, Peck MW. 2005. Heterogeneity of times required for germination and outgrowth from single spores of nonproteolytic Clostridium botulinum. Appl. Environ. Microbiol. 71:4998–5003 [Google Scholar]
  131. Stringer SC, Webb MD, Peck MW. 2009. Contrasting effects of heat treatment and incubation temperature on germination and outgrowth of individual spores of nonproteolytic Clostridium botulinum bacteria. Appl. Environ. Microbiol. 75:2712–19 [Google Scholar]
  132. Stringer SC, Webb MD, Peck MW. 2011. Lag time variability in individual spores of Clostridium botulinum. Food Microbiol. 28:228–35 [Google Scholar]
  133. Sunde EP, Setlow P, Hederstedt L, Halle B. 2009. The physical state of water in bacterial spores. PNAS 106:19334–39 [Google Scholar]
  134. Talukdar PK, Olguín-Araneda V, Alnoman M, Paredes-Sabja D, Sarker MR. 2015. Updates on the sporulation process in Clostridium species. Res. Microbiol. 166:4225–35 [Google Scholar]
  135. Touw WG, Bayjanov JR, Overmars L, Backus L, Boekhorst J. et al. 2013. Data mining in the Life Sciences with Random Forest: a walk in the park or lost in the jungle?. Brief Bioinform. 14:3315–26 [Google Scholar]
  136. van Asselt ED, Zwietering MH. 2006. A systematic approach to determine global thermal inactivation parameters for various food pathogens. Int. J. Food Microbiol. 107:73–82 [Google Scholar]
  137. van Bokhorst-van de Veen H, Xie H, Esveld E, Abee T, Mastwijk H, Nierop Groot M. 2015. Inactivation of chemical and heat-resistant spores of Bacillus and Geobacillus by nitrogen cold atmospheric plasma evokes distinct changes in morphology and integrity of spores. Food Microbiol. 45:Pt. A26–33 [Google Scholar]
  138. van der Voort M, Abee T. 2013. Sporulation environment of emetic toxin-producing Bacillus cereus strains determines spore size, heat resistance and germination capacity. J. Appl. Microbiol. 114:1201–10 [Google Scholar]
  139. van der Voort M, García D, Moezelaar R, Abee T. 2010. Germinant receptor diversity and germination responses of four strains of the Bacillus cereus group. Int. J. Food Microbiol. 139:108–15 [Google Scholar]
  140. van Melis CC, Almeida CB, Kort R, Groot MN, Abee T. 2012. Germination inhibition of Bacillus cereus spores: impact of the lipophilic character of inhibiting compounds. Int. J. Food Microbiol. 160:124–30 [Google Scholar]
  141. van Melis CC, den Besten HMW, Nierop Groot MN, Abee T. 2014. Quantification of the impact of single and multiple mild stresses on outgrowth heterogeneity of Bacillus cereus spores. Int. J. Food Microbiol. 177:57–62 [Google Scholar]
  142. van Melis CC, Nierop Groot MN, Abee T. 2011. Impact of sorbic acid on germinant receptor-dependent and -independent germination pathways in Bacillus cereus. Appl. Environ. Microbiol. 77:2552–54 [Google Scholar]
  143. van Zuijlen A, Periago PM, Amézquita A, Palop A, Brul S, Fernández PS. 2010. Characterization of Bacillus sporothermodurans IC4 spores; putative indicator microorganism for optimisation of thermal processes in food sterilisation. Food Res. Int. 43:1895–901 [Google Scholar]
  144. Veening JW, Hamoen LW, Kuipers OP. 2005. Phosphatases modulate the bistable sporulation gene expression pattern in Bacillus subtilis. Mol. Microbiol. 56:61481–94 [Google Scholar]
  145. Velásquez J, Schuurman-Wolters G, Birkner JP, Abee T, Poolman B. 2014. Bacillus subtilis spore protein SpoVAC functions as a mechanosensitive channel. Mol. Microbiol. 92:813–23 [Google Scholar]
  146. Visick JE, Clarke S. 1995. Repair, refold, recycle: how bacteria can deal with spontaneous and environmental damage to proteins. Mol. Microbiol. 16:5835–45 [Google Scholar]
  147. Wang G, Zhang P, Setlow P, Li YQ. 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. 77:3368–79 [Google Scholar]
  148. Warda AK, den Besten HMW, Sha N, Abee T, Nierop Groot MN. 2015. Influence of food matrix on outgrowth heterogeneity of heat damaged Bacillus cereus spores. Int. J. Food Microbiol. 201:27–34 [Google Scholar]
  149. Warth AD. 1978. Relationship between the heat resistance of spores and the optimum and maximum growth temperatures of Bacillus species. J. Bacteriol. 134:699–705 [Google Scholar]
  150. Webb MD, Pin C, Peck MW, Stringer SC. 2007. Historical and contemporary NaCl concentrations affect the duration and distribution of lag times from individual spores of nonproteolytic Clostridium botulinum. Appl. Environ. Microbiol. 73:2118–27 [Google Scholar]
  151. Wu AR, Neff NF, Kalisky T, Dalerba P, Treutlein B. et al. 2014. Quantitative assessment of single-cell RNA-sequencing methods. Nat Methods. 11:141–46 [Google Scholar]
  152. Xiao Y, Francke C, Abee T, Wells-Bennik MHJ. 2011. Clostridial spore germination versus bacilli: genome mining and current insights. Food Microbiol. 28:2266–74 [Google Scholar]
  153. Xiao Y, Wagendorp A, Abee T, Wells-Bennik MHJ. 2015. Differential outgrowth potential of Clostridium perfringens food-borne isolates with various cpe-genotypes in vacuum-packed ground beef during storage at 12°C. Int. J. Food Microbiol. 194:40–45 [Google Scholar]
  154. Xiao Y, Wagendorp A, Moezelaar R, Abee T, Wells-Bennik MHJ. 2012. A wide variety of Clostridium perfringens type A food-borne isolates that carry a chromosomal cpe gene belong to one multilocus sequence typing cluster. Appl. Environ. Microbiol. 78:197060–68 [Google Scholar]
  155. Yi X, Setlow P. 2010. Studies of the commitment step in the germination of spores of Bacillus species. J. Bacteriol. 192:3424–33 [Google Scholar]
  156. Young JW, Locke JC, Altinok A, Rosenfeld N, Bacarian T. et al. 2012. Measuring single-cell gene expression dynamics in bacteria using fluorescence time-lapse microscopy. Nat. Protoc. 7:80–88 [Google Scholar]
  157. Zernike F. 1955. How I discovered phase contrast. Science 121:3141345–49 [Google Scholar]
  158. Zhang JQ, Griffiths KK, Cowan A, Setlow P, Yu J. 2013. Expression level of Bacillus subtilis germinant receptors determines the average rate but not the heterogeneity of spore germination. J. Bacteriol. 195:81735–40 [Google Scholar]
  159. Zhang P, Kong L, Wang G, Scotland M, Ghosh S. et al. 2012. Analysis of the slow germination of multiple individual superdormant Bacillus subtilis spores using multifocus Raman microspectroscopy and differential interference contrast microscopy. J. Appl. Microbiol. 112:3526–36 [Google Scholar]
  160. Zwietering MH, den Besten HMW. 2011. Modelling: one word for many activities and uses. Food Microbiol. 28:818–22 [Google Scholar]
  161. Zwietering MH, Wijtzes T, de Wit JC, van‘t Riet K. 1992. A decision support system for prediction of the microbial spoilage in foods. J. Food Prot. 55:973–79 [Google Scholar]
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