Recovery of heat treated Bacillus cereus spores is affected by matrix composition and factors with putative functions in damage repair

Frontiers in Microbiology

Volumn 7, Issue JUL, 2016, Pages

  Warda, Alicja K ^a,b   Tempelaars, Marcel H ^b   Abee, Tjakko ^a,b   Nierop Groot, Masja N ^a,b  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Food matrix; germination and outgrowth; Recovery of spores; Rice; Spore former; Thermal treatment

Indexed keywords

ARTICLE; BACILLUS CEREUS; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL SPORE; BACTERIUM MUTANT; CELL DAMAGE; CELL REGENERATION; CELL SELECTION; CELL SURVIVAL; COLONY FORMATION; COLONY FORMING UNIT; CONTROLLED STUDY; CULTURE MEDIUM; DELETION MUTANT; FLOW CYTOMETRY; GENE EXPRESSION; HEAT TREATMENT; MOST PROBABLE NUMBER METHOD; NONHUMAN; PHASE CONTRAST MICROSCOPY; POLYMERASE CHAIN REACTION; SPORE GERMINATION; SPOROGENESIS; TRANSCRIPTOMICS;

EID: 84983059065     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01096     Document Type: Article

References (49)

1. Abee, T., Wels, M., De Been, M., and Den Besten, H. M. W. (2011). From transcriptional landscapes to the identification of biomarkers for robustness. Microb. Cell Fact. 10(Suppl 1), S9. doi: 10.1186/1475-2859-10-s1-s9
2. Adams, D. M. (1973). "Heat injury of bacterial spores," in Advances in Applied Microbiology, ed. D. Perlman (Cambridge, MA: Academic Press), 245-261.
3. Aguirre, J. S., Ordonez, J. A., and Garcia De Fernando, G. D. (2012). A comparison of the effects of E-beam irradiation and heat treatment on the variability of Bacillus cereus inactivation and lag phase duration of surviving cells. Int. J. Food Microbiol. 153, 444-452. doi: 10.1016/j.ijfoodmicro.2011.12.012
4. Andersson, A., Rönner, U., and Granum, P. E. (1995). What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens? Int. J. Food Microbiol. 28, 145-155. doi: 10.1016/0168-1605(95)00053-4
5. Ayora, S., Stiege, A. C., and Alonso, J. C. (1997). RecR is a zinc metalloprotein from Bacillus subtilis 168. Mol. Microbiol. 23, 639-647. doi: 10.1046/j.1365-2958.1997.2431611.x
6. Bay, D. C., and Turner, R. J. (2009). Diversity and evolution of the small multidrug resistance protein family. BMC Evol. Biol. 9:140. doi: 10.1186/1471-2148-9-140
7. Berendsen, E. M., Boekhorst, J., Kuipers, O. P., and Wells-Bennik, M. H. (2016). A mobile genetic element profoundly increases heat resistance of bacterial spores. ISME J. doi: 10.1038/ismej.2016.59 [Epub ahead of print].
8. Carlin, F., Girardin, H., Peck, M. W., Stringer, S. C., Barker, G. C., Martinez, A., et al. (2000). Research on factors allowing a risk assessment of spore-forming pathogenic bacteria in cooked chilled foods containing vegetables: a FAIR collaborative project. Int. J. Food Microbiol. 60, 117-135. doi: 10.1016/S0168-1605(00)00304-4
9. Cazemier, A. E., Wagenaars, S. F. M., and Ter Steeg, P. F. (2001). Effect of sporulation and recovery medium on the heat resistance and amount of injury of spores from spoilage bacilli. J. Appl. Microbiol. 90, 761-770. doi: 10.1046/j.1365-2672.2001.01302.x
10. Chakraborty, T., Leimeister-Wachter, M., Domann, E., Hartl, M., Goebel, W., Nichterlein, T., et al. (1992). Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J. Bacteriol. 174, 568-574.
11. Checinska, A., Paszczynski, A., and Burbank, M. (2015). Bacillus and other spore-forming genera: variations in responses and mechanisms for survival. Annu. Rev. Food Sci. Technol. 6, 351-369. doi: 10.1146/annurev-food-030713-092332
12. Chen, H. J., Tsai, T. K., Pan, S. C., Lin, J. S., Tseng, C. L., and Shaw, G. C. (2010). The master transcription factor Spo0A is required for poly(3-hydroxybutyrate) (PHB) accumulation and expression of genes involved in PHB biosynthesis in Bacillus thuringiensis. FEMS Microbiol. Lett. 304, 74-81. doi: 10.1111/j.1574-6968.2010.01888.x
13. Choma, C., Guinebretière, M. H., Carlin, F., Schmitt, P., Velge, P., Granum, P. E., et al. (2000). Prevalence, characterization and growth of Bacillus cereus in commercial cooked chilled foods containing vegetables. J. Appl. Microbiol. 88, 617-625. doi: 10.1046/j.1365-2672.2000.00998.x
14. Cortezzo, D. E., Koziol-Dube, K., Setlow, B., and Setlow, P. (2004). Treatment with oxidizing agents damages the inner membrane of spores of Bacillus subtilis and sensitizes spores to subsequent stress. J. Appl. Microbiol. 97, 838-852. doi: 10.1111/j.1365-2672.2004.02370.x
15. den Besten, H. M. W., Ingham, C. J., Van Hylckama Vlieg, J. E. T., Beerthuyzen, M. M., Zwietering, M. H., and Abee, T. (2007). Quantitative analysis of population heterogeneity of the adaptive salt stress response and growth capacity of Bacillus cereus ATCC 14579. Appl. Environ. Microbiol. 73, 4797-4804. doi: 10.1128/aem.00404-407
16. Dierick, K., Van Coillie, E., Swiecicka, I., Meyfroidt, G., Devlieger, H., Meulemans, A., et al. (2005). Fatal family outbreak of Bacillus cereus - associated food poisoning. J. Clin. Microbiol. 43, 4277-4279. doi: 10.1128/jcm.43.8.4277-4279.2005
17. Ehling-Schulz, M., Fricker, M., and Scherer, S. (2004). Bacillus cereus, the causative agent of an emetic type of food-borne illness. Mol. Nutr. Food Res. 48, 479-487. doi: 10.1002/mnfr.200400055
18. Faille, C., Lebret, V., Gavini, F., and Maingonnat, J.-F. (1997). Injury and lethality of heat treatment of Bacillus cereus spores suspended in buffer and in poultry meat. J. Food Prot. 60, 544-547.
19. Feeherry, F. E., Munsey, D. T., and Rowley, D. B. (1987). Thermal inactivation and injury of Bacillus stearothermophilus spores. Appl. Environ. Microbiol. 53, 365-370.
20. Gamsjaeger, R., Liew, C. K., Loughlin, F. E., Crossley, M., and Mackay, J. P. (2007). Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem. Sci. 32, 63-70. doi: 10.1016/j.tibs.2006.12.007
21. Garcia, D., Van Der Voort, M., and Abee, T. (2010). Comparative analysis of Bacillus weihenstephanensis KBAB4 spores obtained at different temperatures. Int. J. Food Microbiol. 140, 146-153. doi: 10.1016/j.ijfoodmicro.2010.04.005
22. Ghosh, S., and Setlow, P. (2010). The preparation, germination properties and stability of superdormant spores of Bacillus cereus. J. Appl. Microbiol. 108, 582-590. doi: 10.1111/j.1365-2672.2009.04442.x
23. Granum, P. E. (2005). "Bacillus cereus," in Foodborne Pathogens: Microbiology and Molecular Biology, eds P. M. Fratamico, A. K. Bhunia and J. L. Smith (Caister: Academic Press).
24. Jack, D. L., Storms, M. L., Tchieu, J. H., Paulsen, I. T., and Saier M. H. Jr. (2000). A broad-specificity multidrug eux pump requiring a pair of homologous SMR-type proteins. J. Bacteriol. 182, 2311-2313. doi: 10.1128/JB.182.8.2311-2313.2000
25. Jarvis, B. (2012). "Chapter 1: Some practical and statistical aspects of the comparative evaluation of microbiological culture media," in Handbook of Culture Media for Food and Water Microbiology, 3rd Edn, eds J. E. L. Corry, G. D. W. Curtis and R. M. Baird (London: The Royal Society of Chemistry), 3-38.
26. Kominek, L. A., and Halvorson, H. O. (1965). Metabolism of poly-beta-hydroxybutyrate and acetoin in Bacillus cereus. J. Bacteriol. 90, 1251-1259.
27. Laity, J. H., Lee, B. M., and Wright, P. E. (2001). Zinc finger proteins: new insights into structural and functional diversity. Curr. Opin. Struct. Biol. 11, 39-46. doi: 10.1016/S0959-440X(00)00167-6
28. Lee, T. R., Lin, J. S., Wang, S. S., and Shaw, G. C. (2004). PhaQ, a new class of poly-beta-hydroxybutyrate (PHB)-responsive repressor, regulates phaQ and phaP (phasin) expression in Bacillus megaterium through interaction with PHB. J. Bacteriol. 186, 3015-3021. doi: 10.1128/JB.186.10.3015-3021.2004
29. Mafart, P., Leguerinel, I., Couvert, O., and Coroller, L. (2010). Quantification of spore resistance for assessment and optimization of heating processes: a never-ending story. Food Microbiol. 27, 568-572. doi: 10.1016/j.fm.2010.03.002
30. McCool, G. J., and Cannon, M. C. (1999). Polyhydroxyalkanoate inclusion body-associated proteins and coding region in Bacillus megaterium. J. Bacteriol. 181, 585-592.
31. Moussa-Boudjemaa, B., Gonzalez, J., and Lopez, M. (2006). Heat resistance of Bacillus cereus spores in carrot extract acidified with different acidulants. Food Control 17, 819-824. doi: 10.1016/j.foodcont.2005.05.009
32. Oblinger, J. L., and Koburger, J. A. (1975). Understanding and teaching the most probable number technique. J. Milk Food Technol. 38, 540-545.
33. Pasha, I., Saeed, F., Sultan, M. T., Khan, M. R., and Rohi, M. (2014). Recent developments in minimal processing: a tool to retain nutritional quality of food. Crit. Rev. Food Sci. Nutr. 54, 340-351. doi: 10.1080/10408398.2011.585254
34. Postollec, F., Mathot, A. G., Bernard, M., Divanac'h, M. L., Pavan, S., and Sohier, D. (2012). Tracking spore-forming bacteria in food: from natural biodiversity to selection by processes. Int. J. Food Microbiol. 158, 1-8. doi: 10.1016/j.ijfoodmicro.2012.03.004
35. Rodriguez-Palacios, A., and Lejeune, J. T. (2011). Moist-heat resistance, spore aging, and superdormancy in Clostridium difficile. Appl. Environ. Microbiol. 77, 3085-3091. doi: 10.1128/aem.01589-1510
36. Samapundo, S., Heyndrickx, M., Xhaferi, R., De Baenst, I., and Devlieghere, F. (2014). 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. doi: 10.1016/j.ijfoodmicro.2014.04.018
37. Schoeni, J. L., and Wong, A. C. L. (2005). Bacillus cereus food poisoning and its toxins. J. Food Prot. 68, 636-648.
38. Setlow, P. (2014). Spore resistance properties. Microbiol. Spectr. 2, 1-14. doi: 10.1128/microbiolspec.TBS-0003-2012
39. Slepecky, R. A., and Law, J. H. (1961). Synthesis and degradation of poly-beta-hydroxybutyric acid in connection with sporulation of Bacillus megaterium. J. Bacteriol. 82, 37-42.
40. Smelt, J. P., Bos, A. P., Kort, R., and 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. doi: 10.1016/j.ijfoodmicro.2008.08.023
41. Stecchini, M. L., Del Torre, M., and Polese, P. (2013). Survival strategies of Bacillus spores in food. Indian J. Exp. Biol. 51, 905-909.
42. Stenfors Arnesen, L. P., Fagerlund, A., and Granum, P. E. (2008). From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Rev. 32, 579-606. doi: 10.1111/j.1574-6976.2008.00112.x
43. Stringer, S. C., Webb, M. D., and Peck, M. W. (2011). Lag time variability in individual spores of Clostridium botulinum. Food Microbiol. 28, 228-235. doi: 10.1016/j.fm.2010.03.003
44. van Melis, C. C. J., Den Besten, H. M. W., Nierop Groot, M. N., and 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. doi: 10.1016/j.ijfoodmicro.2014.02.015
45. Wang, G., Zhang, P., Setlow, P., and 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, 3368-3379. doi: 10.1128/aem.00046-11
46. Warda, A. K., Den Besten, H. M. W., Sha, N., Abee, T., and Nierop Groot, M. N. (2015). Influence of food matrix on outgrowth heterogeneity of heat damaged Bacillus cereus spores. Int. J. Food Microbiol. 201, 27-34. doi: 10.1016/j.ijfoodmicro.2015.02.010
47. Warda, A. K., Tempelaars, M. H., Boekhorst, J., Abee, T., and Nierop Groot, M. N. (2016). Identification of cdnl, a putative transcriptional regulator involved in repair and outgrowth of heat-damaged Bacillus cereus Spores. PLoS ONE 11:e0148670. doi: 10.1371/journal.pone.0148670
48. Wells-Bennik, M. H., Eijlander, R. T., Den Besten, H. M., Berendsen, E. M., Warda, A. K., Krawczyk, A. O., et al. (2016). Bacterial spores in food: survival, emergence, and outgrowth. Annu. Rev. Food Sci. Technol. 7, 457-482. doi: 10.1146/annurev-food-041715-33144
49. Wu, V. C. (2008). A review of microbial injury and recovery methods in food. Food Microbiol. 25, 735-744. doi: 10.1016/j.fm.2008.04.011