The heat resistance and spoilage potential of aerobic mesophilic and thermophilic spore forming bacteria isolated from Chinese milk powders

International Journal of Food Microbiology

Volumn 238, Issue , 2016, Pages 193-201

  Sadiq, Faizan A ^a   Li, Yun ^b   Liu, TongJie ^a   Flint, Steve ^c   Zhang, Guohua ^a   Yuan, Lei ^a   Pei, Zhipeng ^a   He, GuoQing ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b HANSHAN NORMAL UNIVERSITY   (China)

^c MASSEY UNIVERSITY   (New Zealand)

Author keywords

Aerobic sporeformers; Milk powder; RAPD; Spoilage enzymes; Thermal resistance

Indexed keywords

BETA GALACTOSIDASE; PHOSPHOLIPASE; POWDER;

AEROBIC BACTERIUM; ARTICLE; BACILLUS CEREUS; BACILLUS LICHENIFORMIS; BACILLUS SUBTILIS; BACTERIUM ISOLATION; BREVIBACILLUS; BREVIBACILLUS BREVIS; CHINA; CONTROLLED STUDY; ELECTRIC POTENTIAL; ENZYME ACTIVITY; FOOD QUALITY; FOOD SPOILAGE; GEOBACILLUS STEAROTHERMOPHILUS; GEOBACILLUS THERMOLEOVORANS; HEAT TOLERANCE; HEMOLYSIS; LIPOLYSIS; MESOPHILIC BACTERIUM; MILK POWDER; NONHUMAN; PAENIBACILLUS MACERANS; PHENOTYPE; PHENOTYPIC VARIATION; PROTEIN DEGRADATION; THERMOPHILIC BACTERIUM; VIRGIBACILLUS; ANALYSIS; ANIMAL; BACTERIAL SPORE; BACTERIUM; CHEMISTRY; CLASSIFICATION; FOOD CONTAMINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; ISOLATION AND PURIFICATION; MICROBIOLOGY; MILK; POWDER; RANDOM AMPLIFIED POLYMORPHIC DNA;

ANIMALS; BACTERIA; CHINA; FOOD CONTAMINATION; HOT TEMPERATURE; MILK; POWDERS; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE; SPORES, BACTERIAL;

EID: 84987984225     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2016.09.009     Document Type: Article

References (72)

1. Abdel-Fattah, Y.R., Gaballab, A.A., Identification and over-expression of a thermostable lipase from Geobacillus thermoleovorans Toshki in Escherichia coli. Microbiol. Res. 163 (2008), 13–20.
2. André, S., Zuber, F., Remize, F., 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 (2013), 134–143.
3. Berendsen, E.M., Zwietering, M.H., Kuipers, O.P., Wells-Bennik, M.H.J., Two distinct groups within the Bacillus subtilis group display significantly different spore heat resistance properties. Food Microbiol. 45 (2015), 18–25.
4. Berendsen, E.M., Krawczyk, A.O., Klaus, V., de Jong, A., Boekhorst, J., Eijlander, R.T., Kuipers, O.P., Wells-Bennik, M.H., Bacillus thermoamylovorans spores with very-high-level heat resistance germinate poorly in rich medium despite the presence of ger clusters but efficiently upon exposure to calcium-dipicolinic acid. Appl. Environ. Microbiol. 81 (2015), 7791–7801.
5. Berendsen, E.M., Boekhorst, J., Kuipers, O.P., Wells-Bennik, M.H., A mobile genetic element profoundly increases heat resistance of bacterial spores. The ISME Journal, 2016, 10.1038/ismej.2016.59.
6. Burgess, S.A., Lindsay, D., Flint, S.H., Thermophilic bacilli and their importance in dairy processing. Int. J. Food Microbiol. 144 (2010), 215–225.
7. Burgess, S.A., Cox, M.P., Flint, S.H., Lindsay, D., Biggs, P.J., Draft genome sequences of three strains of Geobacillus stearothermophilus isolated from a milk powder manufacturing plant. Genome Announcements, 2015, 3, 10.1128/genomeA.00939-15.
8. Caldera, L., Franzetti, L., Van Coillie, E., De Vos, P., Stragier, P., De Block, J., Heyndrickx, M., Identification, enzymatic spoilage characterization and proteolytic activity quantification of Pseudomonas spp. isolated from different foods. Food Microbiol. 54 (2016), 142–153.
9. Cattani, F., Ferreira, C.A.S., Oliveira, S.D., The detection of viable vegetative cells of Bacillus sporothermodurans using propidium monoazide with semi-nested PCR. Food Microbiol. 34 (2013), 196–201.
10. Cazemier, A.E., Wagenaars, S.F.M., ter Steeg, P.F., Effect of sporulation and recovery medium on the heat resistance and amount of injury of spores from spoilage bacilli. J. Appl. Microbiol. 90 (2001), 761–770.
11. Chen, L., Daniel, R.M., Coolbear, T., Detection and impact of protease and lipase activities in milk and milk powders. Int. Dairy J. 13 (2003), 255–275.
12. Chen, L., Coolbear, T., Daniel, R.M., Characteristics of proteinases and lipases produced by seven Bacillus sp. isolated from milk powder production lines. Int. Dairy J. 14 (2004), 495–504.
13. Chopra, A.K., Mathur, D.K., Isolation, screening and characterization of thermophilic Bacillus species isolated from dairy products. J. Appl. Bacteriol. 57 (1984), 263–271.
14. Christiansson, A., Bertilsson, J., Svensson, B., Bacillus cereus spores in raw milk: factors affecting the contamination of milk during the grazing period. J. Dairy Sci. 82 (1999), 305–314.
15. Cogan, T.M., A review of heat resistant lipases and proteinases and the quality of dairy products. Irish J. Food Sci. Technol. 1 (1977), 95–105.
16. Condón, S., Palop, A., Raso, J., Sala, F.J., Influence of the incubation temperature after heat treatment upon the estimated heat resistance values of spores of Bacillus subtilis. Lett. Appl. Microbiol. 22 (1996), 149–152.
17. Davies, F.L., Underwood, H.M., Perkins, A.G., Burton, H., Thermal death kinetics of Bacillus stearothermophilus spores at ultra high temperatures. I. Laboratory determination of temperature coefficients. J. Food Technol. 12 (1977), 115–129.
18. De Jonghe, V., Coorevits, A., De Block, J., Van Coillie, E., Grijspeerdt, K., Herman, L., De Vos, P., Heyndrickx, M., Toxinogenic and spoilage potential of aerobic spore formers isolated from raw milk. Int. J. Food Microbiol. 136 (2010), 318–325.
19. Dhakal, R., Chauhan, K., Seale, R.B., Deeth, H.C., Pillidge, C.J., Powell, I.B., Craven, H., Turner, M.S., Genotyping of dairy Bacillus licheniformis isolates by high resolution melt analysis of multiple variable number tandem repeat loci. Food Microbiol. 34 (2013), 344–351.
20. Dufrenne, J., Bijwaard, M., te Giffel, M., Beumer, R., Notermans, S., Characteristics of some psychrotrophic Bacillus cereus isolates. Int. J. Food Microbiol. 27 (1995), 175–183.
21. Duncan, S.E., Christen, G.L., Sensory detection and recovery by acid degree value of fatty acids added to milk. J. Dairy Sci. 74 (1991), 2855–2859.
22. Durand, L., Planchon, S., Guinebretiere, M.H., Carlin, F., Remize, F., Genotypic and phenotypic characterization of foodborne Geobacillus stearothermophilus. Food Microbiol. 45 (2015), 103–110.
23. Elwan, S.H., Mostafa, S.A., Khodair, A.A., Ali, O., Identity and lipase activity of an isolate of Thermoactinomyces vulgaris. Zentralbl Bakteriol Naturwiss 133 (1978), 713–722.
24. Esteban, M.D., Huertas, J.P., Fernandez, P.S., Palop, A., Effect of the medium characteristics and the heating and cooling rates on the nonisothermal heat resistance of Bacillus sporothermodurans IC4 spores. Food Microbiol. 34 (2013), 158–163.
25. Falkowski, J., Lipolytic activity from milk isolated strains of the species Thermoactinomyces vulgaris, Tsiklinsky 1899 (author's transl). Zentralblatt für Bakteriologie B. 168 (1979), 361–666.
26. Feeherry, F.E., Munsey, D.T., Rowley, D.B., Thermal inactivation and injury of Bacillus stearothermophilus spores. Appl. Environ. Microbiol. 53 (1987), 365–370.
27. Fernández, A., Ocio, M.J., Fernández, P.S., Rodrigo, M., Martinez, A., Application of nonlinear regression analysis to the estimation of kinetic parameters for two enterotoxigenic strains of Bacillus cereus spores. Food Microbiol. 16 (1999), 607–613.
28. Fitz-Gerald, C.H., Deeth, H.C., Factors influencing lipolysis by skim milk cultures of some psychrotrophic microorganisms. Aust. J. Dairy Technol. 38 (1983), 97–103.
29. Flint, S., Palmer, J., Bloemen, K., Brooks, J., Crawford, R., The growth of Bacillus stearothermophilus on stainless steel. J. Appl. Microbiol. 90 (2001), 151–157.
30. Gilmour, A., Rowe, M.T., Micro-organisms associated with milk. Robinson, R.K., (eds.) Dairy Microbiology, 1990, Elsevier Applied Science, London, 37–76.
31. Granum, P.E., Bacillus cereus and Food Poisoning. Berkeley, R.C., Heyndrickx, M., Logan, N.A., De Vos, P., (eds.) Applications and Systematics of Bacillus and Relatives, 2002, Blackwell Science, Oxford, UK, 37–46.
32. Griffiths, M.W., Phillips, J.D., Muir, D.D., Thermostability of proteases and lipases from a number of species of psychrotrophic bacteria of dairy origin. J. Appl. Bacteriol. 50 (1981), 289–303.
33. Harwalkar, V.R., Age gelation of sterlized milks. Fox, P.F., (eds.) Advanced Dairy Chemistry-1: Proteins, 1992, Elsevier Applied Science, London and New York, 691–734.
34. Heyndrickx, M., Scheldeman, P., Bacilli associated with spoilage in dairy and other food products. Berkely, R., Heyndrickx, M., Logan, N.A., De Vos, P., (eds.) Applications and Systematics of Bacillus and Relatives, 2002, Blackwell Science, Oxford, UK, 64–82.
35. Hill, B.M., Smythe, B.W., Endospores of thermophilic bacteria in ingredient milk powders and their significance to the manufacture of sterilized milk products: an industrial perspective. Food Rev. Int. 28 (2012), 299–312.
36. Hoult, B., Tuxford, A.F., Toxin production by Bacillus pumilus. Journal of Clinal Pathology 44 (1991), 455–458.
37. Humbert, G., Guingamp, M.-P., Linden, G., Method for the measurement of lipase activity in milk. J. Dairy Res. 64 (1997), 465–469.
38. Ivy, R.A., Ranieri, M.L., Martin, N.H., den Bakker, H.C., Xavier, B.M., Wiedmann, M., Boor, K.J., Identification and characterization of psychrotolerant sporeformers associated with fluid milk production and processing. Appl. Environ. Microbiol. 78 (2012), 1853–1864.
39. Juajun, O., Nguyen, T.H., Maischberger, T., Iqbal, S., Haltrich, D., Yamabhai, M., Cloning, purification, and characterization of β-galactosidase from Bacillus licheniformis DSM 13. Appl. Microbiol. Biotechnol. 89 (2011), 645–654.
40. Kent, D.J., Chauhan, K., Boor, K.J., Wiedmann, M., Martin, N.H., Spore test parameters matter: Mesophilic and thermophilic spore counts detected in raw milk and dairy powders differ significantly by test method. J. Dairy Sci. 99 (2016), 5180–5191.
41. Koka, R., Weimer, B.C., Influence of growth conditions on heatstable phospholipase activity in Pseudomonas. J. Dairy Res. 68 (2001), 109–116.
42. Krawczyk, A.O., de Jong, A., Holsappel, S., Eijlander, R.T., van Heel, A., Berendsen, E.M., Wells-Bennik, M.H., Kuipers, O.P., Genome sequences of 12 spore-forming Bacillus species, comprising Bacillus coagulans, Bacillus licheniformis, Bacillus amyloliquefaciens, Bacillus sporothermodurans, and Bacillus vallismortis, isolated from foods. Genome Announcements, 4, 2016, 10.1128/genomeA.00103-16.
43. Lücking, G., Stoeckel, M., Atamer, Z., Hinrichs, J., Ehling-Schulz, M., Characterization of aerobic spore-forming bacteria associated with industrial dairy processing environments and product spoilage. Int. J. Food Microbiol. 166 (2013), 270–279.
44. Lundahl, G., A method of increasing test range and accuracy of bioindicators: Geobacillus stearothermophilus spores. PDA J. Pharm. Sci. Technol. 57 (2003), 249–262.
45. Luu-Thi, H., Khadka, D.B., Michiels, C.W., Thermal inactivation parameters of spores from different phylogenetic groups of Bacillus cereus. Int. J. Food Microbiol. 189 (2014), 183–188.
46. Marchand, S., Vandriesche, G., Coorevits, A., Coudijzer, K., De Jonghe, V., Dewettinck, K., De Vos, P., Devreese, B., Heyndrickx, M., De Block, J., Heterogeneity of heat-resistant proteases from milk Pseudomonas species. Int. J. Food Microbiol. 133 (2009), 68–77.
47. Meer, R.R., Bakker, J., Bodyfelt, F.W., Griffiths, M.W., Psychotrophic Bacillus spp. in fluid milk products: a review. J. Food Prot. 54 (1991), 969–979.
48. Nicholson, W.L., Munakata, N., Horneck, G., Melosh, H.J., Setlow, P., Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64 (2000), 548–572.
49. Novak, J.S., Call, J., Tomasula, P., Luchansky, J.B., An assessment of pasteurization treatment of water, media, and milk with respect to Bacillus spores. J. Food Prot. 68 (2005), 751–757.
50. Oomes, S.J.C.M., van Zuijlen, A.C.M., Hehenkamp, J.O., Witsenboer, H., van der Vossen, J.M.B.M., Brul, S., The characterisation of Bacillus spores occurring in the manufacturing of (low acid) canned products. Int. J. Food Microbiol. 120 (2007), 85–94.
51. Palop, A., Mañas, P., Condón, S., Sporulation temperature and heat resistance of Bacillus spores: A review. J. Food Saf. 19 (2007), 57–72.
52. Pearce, L.E., Survey of data on heat resistance of dairy pathogens. Bulletin of the International Dairy Federation 392 (2004), 37–41.
53. Ranieri, M., Huck, J., Sonnen, M., Barbano, D., Boor, K., High temperature, short time pasteurization temperatures inversely affect bacterial numbers during refrigerated storage of pasteurized fluid milk. J. Dairy Sci. 92 (2009), 4823–4832.
54. Rodriguez-Palacios, A., LeJeune, J.T., Moist-heat resistance, spore aging, and superdormancy in Clostridium difficile. Appl. Environ. Microbiol. 77 (2011), 3085–3091.
55. Rombaut, R., Dewettinck, K., De Mangelaere, G., Huyghebaert, A., Inactivation of heat resistant spores in bovine milk and lactulose formation. Milchwissenschaft 57 (2002), 432–436.
56. Sadiq, F.A., Li, Y., Liu, T., Flint, S., Zhang, G., He, G., A RAPD based study revealing a previously unreported wide range of mesophilic and thermophilic spore formers associated with milk powders in China. Int. J. Food Microbiol. 217 (2016), 200–208.
57. Salkinoja-Salonen, M.S., Vuorio, R., Andersson, M.A., Kämpfer, P., Andersson, M.C., Honkanen-Buzalski, T., Scoging, A.C., Toxigenic strains of Bacillus licheniformis related to food poisoning. Appl. Environ. Microbiol. 10 (1999), 4637–4645.
58. Scheldeman, P., Herman, L., Foster, S., Heyndrickx, M., Bacillus sporothermodurans and other highly heat-resistant spore formers in milk. J. Appl. Microbiol. 101 (2006), 542–555.
59. Scott, S.A., Brooks, J.D., Rakonjac, J., Walker, K.M.R., Flint, S.H., The formation of thermophilic spores during the manufacture of whole milk powder. Int. J. Dairy Technol. 60 (2007), 109–117.
60. Shah, N.P., Psychrotrophs in milk: a review. Millchwissenschaft 49 (1994), 432–437.
61. Shamsuzzaman, K., Modler, W., McKellar, R.C., Survival of lipase during manufacture of nonfat dry milk. J. Dairy Sci. 70 (1986), 746–751.
62. Sinchaikul, S., Sookkheo, B., Phutrakul, S., Wu, Y.T., Pan, F.M., Chen, S.T., Structural modeling and characterization of a thermostable lipase from Bacillus stearothermophilus P1. Biochem. Biophys. Res. Commun. 283 (2001), 868–875.
63. Sperber, W.H., Doyle, M.P., Compendium of the Microbiological Spoilage of Foods and Beverages. 2009, Springer Science, New York, NY 367 pp.
64. Stathopoulou, P.M., Savvides, A.L., Karagouni, A.D., Hatzinikolaou, D.G., Unraveling the lipolytic activity of thermophilic bacteria isolated from a volcanic environment. Biomedical Research International, 2013, 2013, 703130.
65. Stoeckel, M., Lidolt, M., Achberger, V., Glück, C., Krewinkel, M., Stressler, T., von Neubeck, M., Wenning, M., Scherer, S., Fischer, L., Hinrichs, J., Growth of Pseudomonas weihenstephanensis, Pseudomonas proteolytica and Pseudomonas sp.in raw milk: impact of residual heat-stable enzyme activity on stability of UHT milk during shelf-life. Int. Dairy J. 59 (2016), 20–28.
66. Teh, K.H., Flint, S., Palmer, J., Andrewes, P., Bremer, P., Lindsay, D., Proteolysis produced within biofilms of bacterial isolates from raw milk tankers. Int. J. Food Microbiol. 157 (2012), 28–34.
67. Tyndall, J.D., Sinchaikul, S., Fothergill-Gilmore, L.A., Taylor, P., Walkinshaw, M.D., Crystal structure of a thermostable lipase from Bacillus stearothermophilus P1. J. Mol. Biol. 323 (2002), 859–869.
68. von Neubeck, M., Baur, C., Krewinkel, M., Stoeckel, M., Kranz, B., Stressler, T., Fischer, L., Hinrichs, J., Scherer, S., Wenning, M., Biodiversity of refrigerated raw milk microbiota and their enzymatic spoilage potential. Int. J. Food Microbiol. 211 (2015), 57–65.
69. Wijnands, L.M., Dufrenne, J.B., van Leusden, F.M., 2005. Bacillus cereus: characteristics, behaviour in the gastro-intestinal tract, and interaction with Caco-2 cells. RIVM report 250912003/2005. (accessed at www.rivm.nl, June 18, 2016).
70. Woods, R.G., Burger, M., Beven, C.A., Beacham, I.R., The aprX–lipA operon of Pseudomonas fluorescens B52: a molecular analysis of metalloprotease and lipase production. Microbiology 147 (2001), 345–354.
71. Xu, S., Labuza, T.P., Diez-Gonzalez, F., Thermal inactivation of Bacillus anthracis spores in cow's milk. Appl. Environ. Microbiol. 72 (2006), 4479–4483.
72. Yuan, D.D., Liu, G.C., Ren, D.Y., Zhang, D., Zha, L., Kan, C.P., Yang, Y.Z., Maa, W., Li, Y., Zhang, L.B., A survey on occurrence of thermophilic bacilli in commercial milk powders in China. Food Control 25 (2012), 752–757.