Characterization of aerobic spore-forming bacteria associated with industrial dairy processing environments and product spoilage

International Journal of Food Microbiology

Volumn 166, Issue 2, 2013, Pages 270-279

  Lücking, Genia ^a   Stoeckel, Marina ^b   Atamer, Zeynep ^b   Hinrichs, Jörg ^b   Ehling Schulz, Monika ^c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF HOHENHEIM   (Germany)

^c UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Cytotoxic potential; Dairy processing environment; Dairy products; Food spoilage; Spore heat resistance; Spore forming bacteria

Indexed keywords

AEROBIC BACTERIUM; ARTICLE; BACILLUS AMYLOLIQUEFACIENS; BACILLUS CEREUS; BACILLUS LICHENIFORMIS; BACILLUS SUBTILIS; BACTERIAL SPORE; BACTERIAL STRAIN; BACTERIUM ISOLATE; BIODIVERSITY; ENZYME ACTIVITY; FOOD PROCESSING; FOOD QUALITY; FOOD SAFETY; FOOD SPOILAGE; GEOBACILLUS STEAROTHERMOPHILUS; HEAT TOLERANCE; INFRARED SPECTROSCOPY; NONHUMAN;

BACILLUS AMYLOLIQUEFACIENS; BACILLUS CEREUS; BACILLUS LICHENIFORMIS; BACILLUS SMITHII; BACILLUS SUBTILIS; GEOBACILLUS PALLIDUS; GEOBACILLUS STEAROTHERMOPHILUS;

EID: 84882960367     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2013.07.004     Document Type: Article

References (60)

1. Ahn J., Balasubramaniam V.M., Yousef A.E. Inactivation kinetics of selected aerobic and anaerobic bacterial spores by pressure-assisted thermal processing. International Journal of Food Microbiology 2007, 113:321-329.
2. Andersson A., Ronner U., Granum P.E. What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens?. International Journal of Food Microbiology 1995, 28:145-155.
3. Apetroaie-Constantin C., Mikkola R., Andersson M.A., Teplova V., Suominen I., Johansson T., Salkinoja-Salonen M. Bacillus subtilis and B. mojavensis strains connected to food poisoning produce the heat stable toxin amylosin. Journal of Applied Microbiology 2009, 106:1976-1985.
4. Beattie S.H., Williams A.G. Detection of toxigenic strains of Bacillus cereus and other Bacillus spp. with an improved cytotoxicity assay. Letters in Applied Microbiology 1999, 28:221-225.
5. Cazemier A.E., Wagenaars S.F., ter Steeg P.F. Effect of sporulation and recovery medium on the heat resistance and amount of injury of spores from spoilage bacilli. Journal of Applied Microbiology 2001, 90:761-770.
6. Chun J., Bae K.S. Phylogenetic analysis of Bacillus subtilis and related taxa based on partial gyrA gene sequences. Antonie Van Leeuwenhoek 2000, 78:123-127.
7. Coorevits A., De Jonghe V., Vandroemme J., Reekmans R., Heyrman J., Messens W., De Vos P., Heyndrickx M. Comparative analysis of the diversity of aerobic spore-forming bacteria in raw milk from organic and conventional dairy farms. Systematic and Applied Microbiology 2008, 31:126-140.
8. Coroller L., Leguerinel I., Mafart P. Effect of water activities of heating and recovery media on apparent heat resistance of Bacillus cereus spores. Applied and Environmental Microbiology 2001, 67:317-322.
9. Crielly E.M., Logan N.A., Anderton A. Studies on the Bacillus flora of milk and milk products. Journal of Applied Bacteriology 1994, 77:256-263.
10. De Clerck E., Vanhoutte T., Hebb T., Geerinck J., Devos J., De Vos P. Isolation, characterization, and identification of bacterial contaminants in semifinal gelatin extracts. Applied and Environmental Microbiology 2004, 70:3664-3672.
11. 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. International Journal of Food Microbiology 2010, 136:318-325.
12. Dietrich R., Fella C., Strich S., Märtlbauer E. Production and characterization of monoclonal antibodies against the hemolysin BL enterotoxin complex produced by Bacillus cereus. Applied and Environmental Microbiology 1999, 65:4470-4474.
13. Dogan Z., Weidendorfer K., Müller-Merbach M., Lembke F., Hinrichs J. Inactivation kinetics of Bacillus spores in batch- and continuous- heating systems. LWT- Food Science and Technology 2009, 42:81-86.
14. Ehling-Schulz M., Messelhäusser U. Bacillus 'next generation' diagnostics: moving from detection towards sub-typing and risk related strain profiling. Frontiers in Microbiology 2013, 4:32. 10.3389/fmicb.2013.00032.
15. Ehling-Schulz M., Fricker M., Scherer S. Bacillus cereus, the causative agent of an emetic type of food-borne illness. Molecular Nutrition & Food Research 2004, 48:479-487.
16. Ehling-Schulz M., Messelhäusser U., Granum P.E. Bacillus cereus in milk and dairy production. Rapid Detection, Characterization and Enumeration of Food-borne Pathogens 2011, 275-289. ASM Press, Washington D.C. J. Hoorfar (Ed.).
17. Fricker M., Skanseng B., Rudi K., Stessl B., Ehling-Schulz M. Shift from farm to dairy tank milk microbiota revealed by a polyphasic approach is independent from geographical origin. International Journal of Food Microbiology 2011, 145:24-30.
18. From C., Pukall R., Schumann P., Hormazabal V., Granum P.E. Toxin-producing ability among Bacillus spp. outside the Bacillus cereus group. Applied and Environmental Microbiology 2005, 71:1178-1183.
19. From C., Hormazabal V., Granum P.E. Food poisoning associated with pumilacidin-producing Bacillus pumilus in rice. International Journal of Food Microbiology 2007, 115:319-324.
20. From C., Hormazabal V., Hardy S.P., Granum P.E. Cytotoxicity in Bacillus mojavensis is abolished following loss of surfactin synthesis: implications for assessment of toxicity and food poisoning potential. International Journal of Food Microbiology 2007, 117:43-49.
21. Heyndrickx M. The importance of endospore-forming bacteria originating from soil for contamination of industrial food processing. Applied and Enviromental Soil Science 2011, 2011. 10.1155/2011/561975.
22. Heyndrickx M., Scheldeman P. Bacilli associated with spoilage in dairy and other food products. Applications and Systematics of Bacillus and Relatives 2002, 64-82. Blackwell Science, Oxford, UK. R. Berkely, M. Heyndrickx, N.A. Logan, P. De Vos (Eds.).
23. Hornstra L.M., Ter Beek A., Smelt J.P., Kallemeijn W.W., Brul S. On the origin of heterogeneity in (preservation) resistance of Bacillus spores: input for a 'systems' analysis approach of bacterial spore outgrowth. International Journal of Food Microbiology 2009, 134:9-15.
24. Hu J.M., Li H., Cao L.X., Wu P.C., Zhang C.T., Sang S.L., Zhang X.Y., Chen M.J., Lu J.Q., Liu Y.H. Molecular cloning and characterization of the gene encoding cold-active beta-galactosidase from a psychrotrophic and halotolerant Planococcus sp. L4. Journal of Agricultural and Food Chemistry 2007, 55:2217-2224.
25. Huck J.R., Hammond B.H., Murphy S.C., Woodcock N.H., Boor K.J. Tracking spore-forming bacterial contaminants in fluid milk-processing systems. Journal of Dairy Science 2007, 90:4872-4883.
26. Huemer I.A., Klijn N., Vogelsang H.W.J., Langeveld L.P.M. Thermal death kinetics of spores of Bacillus sporothermodurans isolated from UHT milk. International Dairy Journal 1998, 8:851-855.
27. Huis in 't Veld J.H. Microbial and biochemical spoilage of foods: an overview. International Journal of Food Microbiology 1996, 33:1-18.
28. 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. Applied and Environmental Microbiology 2012, 78:1853-1864.
29. Kalogridou-Vassiliadou D. Biochemical activities of Bacillus species isolated from flat sour evaporated milk. Journal of Dairy Science 1992, 75:2681-2686.
30. Kort R., O'Brien A.C., van Stokkum I.H., Oomes S.J., Crielaard W., Hellingwerf K.J., Brul S. Assessment of heat resistance of bacterial spores from food product isolates by fluorescence monitoring of dipicolinic acid release. Applied and Environmental Microbiology 2005, 71:3556-3564.
31. Lima L.J., Kamphuis H.J., Nout M.J., Zwietering M.H. Microbiota of cocoa powder with particular reference to aerobic thermoresistant spore-formers. Food Microbiology 2011, 28:573-582.
32. Lima L.J., van der Velpen V., Wolkers-Rooijackers J., Kamphuis H.J., Zwietering M.H., Nout M.J. Microbiota dynamics and diversity at different stages of industrial processing of cocoa beans into cocoa powder. Applied and Environmental Microbiology 2012, 78:2904-2913.
33. Logan N.A. Bacillus and relatives in foodborne illness. Journal of Applied Microbiology 2012, 112:417-429.
34. Lücking G., Dommel M.K., Scherer S., Fouet A., Ehling-Schulz M. Cereulide synthesis in emetic Bacillus cereus is controlled by the transition state regulator AbrB, but not by the virulence regulator PlcR. Microbiology 2009, 155:922-931.
35. Meer R.R., Baker J., Bodyfelt F.W., Griffiths M.W. Psychotrophic Bacillus ssp. in fluid milk products: a review. Journal of Food Protection 1991, 54:969-979.
36. Melly E., Genest P.C., Gilmore M.E., Little S., Popham D.L., Driks A., Setlow P. Analysis of the properties of spores of Bacillus subtilis prepared at different temperatures. Journal of Applied Microbiology 2002, 92:1105-1115.
37. Mikkola R., Kolari M., Andersson M.A., Helin J., Salkinoja-Salonen M.S. Toxic lactonic lipopeptide from food poisoning isolates of Bacillus licheniformis. European Journal of Biochemistry 2000, 267:4068-4074.
38. Mikkola R., Andersson M.A., Grigoriev P., Teplova V.V., Saris N.E., Rainey F.A., Salkinoja-Salonen M.S. Bacillus amyloliquefaciens strains isolated from moisture-damaged buildings produced surfactin and a substance toxic to mammalian cells. Archives of Microbiology 2004, 181:314-323.
39. + channel-forming toxic peptide containing a polyene structure. Toxicon 2007, 49:1158-1171.
40. Nicholson W.L., Setlow P. Sporulation, germination and outgrowth. Molecular Biological Methods for Bacillus 1990, 391-450. C.R. Harwood, S.M. Cutting (Eds.).
41. Oberreuter H., Seiler H., Scherer S. Identification of coryneform bacteria and related taxa by Fourier-transform infrared (FT-IR) spectroscopy. International Journal of Systematic and Evolutionary Microbiology 2002, 52:91-100.
42. Oomes S.J., van Zuijlen A.C., Hehenkamp J.O., Witsenboer H., van der Vossen J.M., Brul S. The characterisation of Bacillus spores occurring in the manufacturing of (low acid) canned products. International Journal of Food Microbiology 2007, 120:85-94.
43. Pettersson B., Lembke F., Hammer P., Stackebrandt E., Priest F.G. Bacillus sporothermodurans, a new species producing highly heat-resistant endospores. International Journal of Systematic Bacteriology 1996, 46:759-764.
44. Phelps R.J., McKillip J.L. Enterotoxin production in natural isolates of Bacillaceae outside the Bacillus cereus group. Applied and Environmental Microbiology 2002, 68:3147-3151.
45. Postollec F., Mathot A.G., Bernard M., Divanac'h M.L., Pavan S., Sohier D. Tracking spore-forming bacteria in food: from natural biodiversity to selection by processes. International Journal of Food Microbiology 2012, 158:1-8.
46. Rowan N.J., Caldow G., Gemmell C.G., Hunter I.S. Production of diarrheal enterotoxins and other potential virulence factors by veterinary isolates of bacillus species associated with nongastrointestinal infections. Applied and Environmental Microbiology 2003, 69:2372-2376.
47. Rückert A., Ronimus R.S., Morgan H.W. A RAPD-based survey of thermophilic bacilli in milk powders from different countries. International Journal of Food Microbiology 2004, 96:263-272.
48. Ryu J.H., Beuchat L.R. Biofilm formation and sporulation by Bacillus cereus on a stainless steel surface and subsequent resistance of vegetative cells and spores to chlorine, chlorine dioxide, and a peroxyacetic acid-based sanitizer. Journal of Food Protection 2005, 68:2614-2622.
49. Salkinoja-Salonen M.S., Vuorio R., Andersson M.A., Kampfer P., Andersson M.C., Honkanen-Buzalski T., Scoging A.C. Toxigenic strains of Bacillus licheniformis related to food poisoning. Applied and Environmental Microbiology 1999, 65:4637-4645.
50. Sanchez-Salas J.L., Setlow B., Zhang P., Li Y.Q., Setlow P. Maturation of released spores is necessary for acquisition of full spore heat resistance during Bacillus subtilis sporulation. Applied and Environmental Microbiology 2011, 77:6746-6754.
51. Scheldeman P., Pil A., Herman L., De Vos P., Heyndrickx M. Incidence and diversity of potentially highly heat-resistant spores isolated at dairy farms. Applied and Environmental Microbiology 2005, 71:1480-1494.
52. Scheldeman P., Herman L., Foster S., Heyndrickx M. Bacillus sporothermodurans and other highly heat-resistant spore formers in milk. Journal of Applied Microbiology 2006, 101:542-555.
53. 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. International Journal of Dairy Technology 2007, 60:109-117.
54. Simmonds P., Mossel B.L., Intaraphan T., Deeth H.C. Heat resistance of Bacillus spores when adhered to stainless steel and its relationship to spore hydrophobicity. Journal of Food Protection 2003, 66:2070-2075.
55. Stenfors Arnesen L.P., Fagerlund A., Granum P.E. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiology Reviews 2008, 32:579-606.
56. Suominen I., Andersson M.A., Andersson M.C., Hallaksela A.M., Kampfer P., Rainey F.A., Salkinoja-Salonen M. Toxic Bacillus pumilus from indoor air, recycled paper pulp, Norway spruce, food poisoning outbreaks and clinical samples. Systematic and Applied Microbiology 2001, 24:267-276.
57. Taylor J.M., Sutherland A.D., Aidoo K.E., Logan N.A. Heat-stable toxin production by strains of Bacillus cereus, Bacillus firmus, Bacillus megaterium, Bacillus simplex and Bacillus licheniformis. FEMS Microbiology Letters 2005, 242:313-317.
58. te Giffel M.C., Wagendorp A., Herrewegh A., Driehuis F. Bacterial spores in silage and raw milk. Antonie Van Leeuwenhoek 2002, 81:625-630.
59. Wenning M., Scherer S., Naumann D. Infrared spectroscopy in the identification of microorganism. Vibrational Spectroscopy for Medical Diagnosis 2008, 71-96. John Wiley & Sons Ltd., Chichester, England. M. Diem, P.R. Griffiths, J.M. Chalmers (Eds.).
60. Witthuhn M., Lücking G., Atamer Z., Ehling-Schulz M., Hinrichs J. Thermal resistance of aerobic spore formers isolated from food products. International Journal of Dairy Technology 2011, 64:486-493.