Environment driven cereulide production by emetic strains of Bacillus cereus

International Journal of Food Microbiology

Volumn 127, Issue 1-2, 2008, Pages 60-67

  Apetroaie Constantin, Camelia ^a   Shaheen, Ranad ^a   Andrup, Lars ^b   Smidt, Lasse ^b   Rita, Hannu ^a   Salkinoja Salonen, Mirja ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b NATIONAL RESEARCH CENTRE FOR THE WORKING ENVIRONMENT   (Denmark)

Author keywords

Cereulide; ces plasmid; Food additive; Glycine; K+ homeostasis; Potassium

Indexed keywords

CEREULIDE;

ARTICLE; BACILLUS CEREUS; BACTERIAL STRAIN; CEREULIDE SYNTHASE GENE; CHEMICAL ANALYSIS; CONTROLLED STUDY; CULTURE MEDIUM; DOWN REGULATION; FOOD CONTAMINATION; FOOD POISONING; GENE; GENETIC ANALYSIS; NONHUMAN;

BACILLUS CEREUS; CONSUMER PRODUCT SAFETY; CULTURE MEDIA; DEPSIPEPTIDES; FOOD CONTAMINATION; FOOD HANDLING; FOOD MICROBIOLOGY; FOOD POISONING; GLYCINE; HUMANS; POTASSIUM; RISK ASSESSMENT; SODIUM; TEMPERATURE;

BACILLUS CEREUS;

EID: 50649114646     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2008.06.006     Document Type: Article

References (66)

1. Agata N., Mori M., Ohta M., Suwan S., Ohtani I., and Isobe M. A novel dodecadepsipeptide, cereulide, isolated from Bacillus cereus causes vacuole formation in HEp-2 cells. FEMS Microbiology Letters 121 (1994) 31-34
2. Agata N., Ohta M., Mori M., and Isobe M. A novel dodecadepsipeptide, cereulide, is an emetic toxin of Bacillus cereus. FEMS Microbiology Letters 129 (1995) 17-20
3. Agata N., Ohta M., and Yokoyama K. Production of Bacillus cereus emetic toxin (cereulide) in various foods. International Journal Food Microbiology 73 (2002) 23-27
4. Andersson M.A., Mikkola R., Helin J., Andersson M.C., and Salkinoja-Salonen M. A novel sensitive bioassay for detection of Bacillus cereus emetic toxin and related depsipeptide ionophores. Applied and Environmental Microbiology 64 (1998) 1338-1343
5. Andersson M.A., Jääskeläinen E.L., Shaheen R., Pirhonen T., Wijnands L.M., and Salkinoja-Salonen M.S. Sperm bioassay for rapid detection of cereulide-producing Bacillus cereus in food and related environments. International Journal of Food Microbiology 94 (2004) 175-183
6. Andersson M.A., Hakulinen P., Honkalampi-Hämäläinen U., Hoornstra D., Lhuguenot J.C., Mäki-Paakkanen J., Savolainen M., Severin I., Stammati A.L., Turco L., Weber A., von Wright A., Zucco F., and Salkinoja-Salonen M. Toxicological profile of cereulide, the Bacillus cereus emetic toxin, in functional assays with human, animal and bacterial cells. Toxicon 49 (2007) 351-367
7. Andrup L., Damgaard J., and Wassermann K. Mobilization of small plasmids in Bacillus thuringiensis subsp. israelensis is accompanied by specific aggregation. Journal of Bacteriology 175 (1993) 6530-6536
8. Apetroaie C., Andersson M.A., Spröer C., Tsitko I., Shaheen R., Jääskeläinen E.L., Wijnands L.M., Heikkilä R., and Salkinoja-Salonen M.S. Cereulide-producing strains of Bacillus cereus show diversity. Archives of Microbiology 184 (2005) 141-151
9. Arnesen L.P., Fagerlund A., and Granum P.E. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiology Reviews (2008) 1-28 10.1111/j.1574-6976.2008.00112.x (online: 16-Apr-2008)
10. Becker B., and Becker H. Epidemiologie. (Epidemiology, in German). In: Becker B. (Ed). Bacillus cereus (2005), B. Behr's Verlag GmbH, Hamburg 23-33
11. Berney M., Weilenmann H.-U., and Egli T. Gene expression of Escherichia coli in continuous culture during adaptation to artificial sunlight. Environmental Microbiology 8 (2006) 1635-1647
12. Carlin F., Fricker M., Pielaat A., Heisterkamp S., Shaheen R., Salkinoja-Salonen M.S., Svensson B., Nguyen-The C., and Ehling-Schulz M. Emetic toxin-producing strains of Bacillus cereus show distinct characteristics within the Bacillus cereus group. International Journal of Food Microbiology 109 (2006) 132-138
13. CLSI, 2006a. Performance standards for antimicrobial disk susceptibility tests; approved standard-9th edition (ANSI/CLSI M2-A9-2006) Clinical and Laboratory Standards Institute, Wayne, PA, USA.
14. CLSI, 2006b. Performance standards for antimicrobial susceptibility testing; sixteenth informational supplement (M100-S16), approved standard-9th ed. Clinical and Laboratory Standards Institute, Wayne, PA, USA.
15. Collett D. Computer software for modelling binary data. In: Collett D. (Ed). Modelling Binary Data (1996), Chapman & Hall, London New York Tokyo 284-340
16. Csonka L.N., and Hanson A.D. Prokaryotic osmoregulation. Genetics and physiology. Annual Review of Microbiology 45 (1991) 569-606
17. Cuin A.G., and Shabala S. Amino acids regulate salinity induced potassium efflux in barley root epidermidis. Planta 225 (2007) 753-761
18. DeFeudis F.V. Amino acids as central neurotransmitters. Annual Reviews of Pharmacology 15 (1975) 105-130
19. Dierick K., Van Coillie E., Swiecicka I., Meyfroidt G., Devlieger H., Meulemans A., Hoedemaekers G., Fourie L., Heyndrickx M., and Mahillon J. Fatal family outbreak of Bacillus cereus-associated food poisoning. Journal of Clinical Microbiology 43 (2005) 4277-4279
20. Ehling-Schulz M., Fricker M., and Scherer S. Identification of emetic toxin producing Bacillus cereus strains by a novel molecular assay. FEMS Microbiology Letters, 232 (2004) 189-195
21. Ehling-Schulz M., Vukov N., Schulz A., Shaheen R., Andersson M., Martlbauer E., and Scherer S. Identification and partial characterization of the nonribosomal peptide synthetase gene responsible for cereulide production in emetic Bacillus cereus. Applied and Environmental Microbiology 71 (2005) 105-113
22. Ehling-Schulz M., Fricker M., Grallert H., Rieck P., Wagner M., and Scherer S. Cereulide synthetase gene cluster from emetic Bacillus cereus: structure and location on a mega virulence plasmid related to Bacillus anthracis toxin plasmid pXO1. BMC Microbiology 6 (2006) 20
23. EU, 1995, 1996, 1998, 2001. Directive 95/2 EC of 20 February, 1995, on Food Additives other than Colours and Sweeteners, amended by directives 96/85/EC, 98/72/EC and 2001/5/EC.
24. EU. Official Journal of the European Communities; Commission Directive 98/64/EC of 3 September 1998 Establishing Community Methods of Analysis for the Determination of Amino Acids, Crude Oils and Fats, and Olaquindox in Feeding Stuffs and Amending Directive 71/393/EEC, Annex 4 (1999), Office for Official Publications of the European Communities, Luxembourg
25. FDA. U.S. Food and Drug Administration. Food and Drugs (Title 21, Volume 3, Revised as of April 1, 2006), Part 170, Food Additives. http://www.accessdata.fda.gov/. Accessed July 3, 2007.
26. Finlay W.J.J., Logan N.A., and Sutherland A.D. Bacillus cereus produces most emetic toxin at lower temperatures. Letters in Applied Microbiology 31 (2000) 385-389
27. Granum P.E. Bacillus cereus. In: Doyle M.P., Beuchat L.R., and Montville T.J. (Eds). Food microbiology Fundamentals and frontiers. 3rd Edition (2007), ASM Press, Washington D.C. 445-456
28. Guinebretière M.H., Broussolle V., and Nguyen-The C. Enterotoxigenic Profiles of food poisoning and food-borne Bacillus cereus strains. Journal of Clinical Microbiology 40 8 (2002) 3053-3056
29. Harvey R.J., and Betz H. Structure, diversity, pharmacology and pathology of glycine receptor chloride channels. In: Endo M. (Ed). Handbook of Experimental Pharamacology vol. 147 (2000), Springer Verlag, Berlin 479-497
30. Hoornstra D., Andersson M.A., Mikkola R., and Salkinoja-Salonen M.S. A new method for in vitro detection of microbially produced mitochondrial toxins. Toxicology In Vitro 17 (2003) 745-751
31. Hoornstra D., Dahlman O., Jääskeläinen E., Andersson M.A., Aurela B., Lindell H., and Salkinoja-Salonen M.S. Retention of Bacillus cereus and its toxin, cereulide, in cellulosic fibres. Holzforschung 60 (2006) 648-652
32. Hornstra L.M., Leeuw P.L.A., Moezelaar R., Wolbert E.J., de Vries Y.P., de Vos W.M., and Abee T. Germination of Bacillus cereus spores adhered to stainless steel. International Journal of Food Microbiology 116 (2007) 367-371
33. Hoton F.M., Andrup L., Swiecicka I., and Mahillon J. The cereulide genetic determinants of emetic Bacillus cereus are plasmid-borne. Microbiology 151 (2005) 2121-2124
34. Häggblom M.M., Apetroaie C., Andersson M.A., and Salkinoja-Salonen M.S. Quantitative analysis of cereulide, the emetic toxin of Bacillus cereus, produced under various conditions. Applied and Environmental Microbiology 68 (2002) 2479-2483
35. Jay J.M., Loessner M.J., and Golden D.A. Bacillus cereus gastroenteritis. Modern Food Microbiology. Seventh Edition (2005), Springer Science + Business Media, Inc., New York, USA 583-590
36. Jensen G.B., Wilcks A., Petersen S.S., Damgaard J., Baum J.A., and Andrup L. The genetic basis of the aggregation system in Bacillus thuringiensis subsp. israelensis is located on the large conjugative plasmid pXO16. Journal of Bacteriology 177 10 (1995) 2914-2917
37. Jääskeläinen E.L., Häggblom M.M., Andersson M.A., Vanne L., and Salkinoja-Salonen M.S. Potential of Bacillus cereus for producing an emetic toxin, cereulide, in bakery products: quantitative analysis by chemical and biological methods. Journal of Food Protection 66 (2003) 1047-1054
38. Jääskeläinen E.L., Häggblom M.M., Andersson M.A., and Salkinoja-Salonen M.S. Atmospheric oxygen and other conditions affecting the production of cereulide by Bacillus cereus in food. International Journal of Food Microbiology 96 (2004) 75-83
39. Kleer J., Bartholoma A., Levetzow R., Reiche T., Sinell H.-J., and Teufel P. Bakterielle Lebensmittel-infektionen und -intoxikationen in Einrichtungen zur gemeinschaftsverpflegung 1985 bis 2000. Archiv für Lebensmittelhygiene 52 (2003) 76-79 (Bacterial infection and intoxication of foods in institutional care from 1985 to 2000, in German)
40. Mahler H., Pasi A., Kramer J.M., Schulte P., Scoging A.C., Bar W., and Krähenbuhl S. Fulminant liver failure in association with the emetic toxin of Bacillus cereus. New England Journal of Medicine 336 (1997) 1142-1148
41. Mayer M.L., and Armstrong N. Structure and function of glutamate receptor ion channels. Annual Reviews of Physiology 66 (2004) 161-181
42. Mikkola R., Saris N.E., Grigoriev P.A., Andersson M.A., and Salkinoja-Salonen M.S. Ionophoretic properties and mitochondrial effects of cereulide, the emetic toxin of Bacillus cereus. European Journal of Biochemistry 263 (1999) 112-117
43. Monaghan D.T., Bridges R.J., and Cotman C.W. The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annual Reviews of Pharmacology and Toxicology, 29 (1989) 365-402
44. Nishikawa Y., Kramer J.M., Hanaoka M., and Yasukawa A. Evaluation of serotyping, biotyping, plasmid banding pattern analysis, and Hep-2 vacuolation factor assay in the epidemiological investigation of Bacillus cereus emetic-syndrome food poisoning. International Journal of Food Microbiology 31 (1996) 149-159
45. Niskanen, T., Johansson, T., Kuusi, M., Raahenmaa, M., Siitonen, A., Tuominen, P. EVIRA, 2006. Ruokamyrkytykset Suomessa vuonna 2005 (Food intoxications in Finland in 2005, in Finnish, with summary and figure legends in English). http://www.evira.fi, Helsinki: The Finnish Food Safety Authority (EVIRA) and University of Helsinki, Evira publication 2/2006, Helsinki, 52 p.
46. NMKL (Nordic Committee on Food Analysis). Determination of metals by atomic absorption spectrophotometry in foodstuffs. Standard protocol #139 (1991)
47. Nordic Working Group on Food Toxicology and Risk Assessment. Nordic Food Additive Database. NNT Report 2002. E640 Glycine and its sodium salt (2002). http://www.foodcomp.dk/foodadd/FoodAddDetails.asp http://www.foodcomp.dk/foodadd/FoodAddDetails.asp. Accessed July 2nd, 2007
48. Pirhonen T., Andersson M.A., Jääskeläinen E.L., Salkinoja-Salonen M.S., Honkanen-Buzalski T., and Johansson T.M. Biochemical and toxic diversity of Bacillus cereus in a pasta and meat dish associated with a food-poisoning case. Food Microbiology 22 (2005) 87-91
49. Rajkovic A., Uyttendaele M., Deley W., Van Soom A., Rijsselaere T., and Debevere J. Dynamics of boar semen motility inhibition as a semi-quantitative measurement of Bacillus cereus emetic toxin (Cereulide). Journal of Microbiological Methods 65 (2006) 525-534
50. Rajkovic A., Uyttendaele M., Ombregt S.A., Jääskeläinen E., Salkinoja-Salonen M., and Debevere J. Influence of type of food on the kinetics and overall production of Bacillus cereus emetic toxin. Journal of Food Protection 69 (2006) 847-852
51. Rajkovic A., Uyttendaele M., Vermeulen A., Andjelkovic M., Fitz-James I., in 't Veld P., Denon Q., Vérhe R., and Debevere J. Heat resistance of Bacillus cereus emetic toxin, cereulide. Letters in Applied Microbiology, 46 (2008) 536-541
52. Raju K.K., Gautam S., and Sharma A. Molecules involved in the modulation of rapid cell death in Xanthomonas. Journal of Bacteriology 188 (2006) 5408-5414
53. Rasko D.A., Rosovitz M.J., Økstad O.A., Fouts D.E., Jiang L., Cer R.Z., Kolstø A.B., Gill S.R., and Ravel J. Complete sequence analysis of novel plasmids from emetic and periodontal Bacillus cereus isolates reveals a common evolutionary history among the B. cereus-group plasmids, including Bacillus anthracis pXO1. Journal of Bacteriology 189 (2007) 52-64
54. Reiche T. Foodborne diseases in communal catering. 5th World Congress Foodborne Infections and Intoxications, Proceedings vol. 1 (2004), Federal Institute for Risk Assessment, Berlin 243-250
55. 15N natural abundance of foliage and soil across the boreal forests of Finland. Biogeochemistry, 80 (2006) 279-288
56. Sakurai N., Koike K.A., Irie Y., and Hayashi H. The rice culture filtrate of Bacillus cereus isolated from emetic-type food poisoning causes mitochondrial swelling in a HEp-2 cell. Microbiology and Immunology 38 (1994) 337-343
57. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd ed. (1989), Cold Spring Harbor Laboratory Press, New York
58. Shaheen R., Andersson M.A., Apetroaie C., Schulz A., Ehling-Schulz M., Ollilainen V.M., and Salkinoja-Salonen M.S. Potential of selected infant food formulas for production of Bacillus cereus emetic toxin, cereulide. International Journal of Food Microbiology 107 (2006) 287-294
59. Shinagawa K., Konuma H., Sekita H., and Sugii S. Emesis of rhesus monkeys induced by intragastric administration with the HEp-2 vacuolation factor (cereulide) produced by Bacillus cereus. FEMS Microbiology Letters 130 (1995) 87-90
60. Szabo R.A., Speirs J.I., and Akhtar M. Cell culture detection and conditions for production of a Bacillus cereus heat-stable toxin. Journal of Food Protection 54 (1991) 272-276
61. Teplova V.V., Mikkola R., Tonshin A.A., Saris N.-E.L., and Salkinoja-Salonen M.S. The higher toxicity of cereulide relative to valinomycin is due to its higher affinity for potassium at physiological plasma concentration. Toxicology and Applied Pharmacology 210 (2006) 39-46
62. Thorsen L., Hansen B.M., Nielsen K.F., Hendriksen N.B., Phipps R.K., and Budde B.B. Characterization of emetic Bacillus weihenstephanensis, a new cereulide-producing bacterium. Applied and Environmental Microbiology 72 (2006) 5118-5121
63. Van der Auwera G.A., Timmery S., Hoton F., and Mahillon J. Plasmid exchanges among members of the Bacillus cereus group in foodstuffs. International Journal of Food Microbiology 113 (2007) 164-172
64. Vilas-Bôas G.T., Peruca A.S.P., and Arantes O.M.N. Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis. Canadian Journal of Microbiology 53 (2007) 673-687
65. Wijnands L.M., Dufrenne J.B., Rombouts F.M., in't Veld P.H., and van Leusden F.M. Prevalence of potentially pathogenic Bacillus cereus in food commodities in The Netherlands. Journal of Food Protection 69 (2006) 2587-2594
66. Wijnands L.M., Dufrenne J.B., Van Leusden F.M., and Abee T. Germination of Bacillus cereus spores is induced by germinants from differentiated Caco2 cells, a human cell line mimicking the epithelial cells of the small intestine. Applied and Environmental Microbiology 73 (2007) 5052-5054