Detection of Bacillus cereus with enteropathogenic potential by multiplex real-time PCR based on SYBR green I

Molecular and Cellular Probes

Volumn 24, Issue 3, 2010, Pages 124-130

  Wehrle, Esther ^a   Didier, Andrea ^a   Moravek, Maximilian ^a   Dietrich, Richard ^a   Märtlbauer, Erwin ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Bacillus cereus; Cereulide; Enterotoxin; Food safety; Multiplex real time PCR; SYBR green I

Indexed keywords

CEREULIDE; CYANINE DYE; CYTOTOXIN; ENTEROTOXIN; HEMOLYSIN;

ARTICLE; BACILLUS CEREUS; BACILLUS LICHENIFORMIS; BACILLUS SUBTILIS; BACILLUS THURINGIENSIS; BACTERIAL COUNT; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM CONTAMINATION; BACTERIUM IDENTIFICATION; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOTOXICITY TEST; DIARRHEA; ENTEROBACTER SAKAZAKII; ENTEROCOCCUS FAECIUM; ESCHERICHIA COLI; GASTROINTESTINAL INFECTION; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; IMMUNOASSAY; LISTERIA MONOCYTOGENES; MELTING POINT; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEUS MIRABILIS; PSEUDOMONAS AERUGINOSA; REAL TIME POLYMERASE CHAIN REACTION; RELIABILITY; SALMONELLA INFANTIS; SENSITIVITY AND SPECIFICITY; STAPHYLOCOCCUS AUREUS; VOMITING;

BACILLUS CEREUS; BACTERIAL PROTEINS; DIARRHEA; DNA PRIMERS; DNA, BACTERIAL; FOOD MICROBIOLOGY; HEMOLYSIN PROTEINS; HUMANS; ORGANIC CHEMICALS; POLYMERASE CHAIN REACTION; SPECIES SPECIFICITY; TRANSITION TEMPERATURE;

BACILLI (CLASS); BACILLUS (BACTERIUM); BACILLUS CEREUS; BACILLUS CEREUS GROUP; BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

EID: 77952243716     PISSN: 08908508     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcp.2009.11.004     Document Type: Article

References (43)

1. Kotiranta A., Lounatmaa K., Haapasalo M. Epidemiology and pathogenesis of Bacillus cereus infections. Microbes Infect 2000, 2:189-198.
2. DGE. Mikrobiologische Aspekte der Ernährung. Ernährungsbericht 2008; Kapitel 5.
3. Schoeni J.L., Wong A.C. Bacillus cereus food poisoning and its toxins. J Food Prot 2005, 68:636-648.
4. Stenfors Arnesen L.P., Fagerlund A., Granum P.E. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 2008, 32:579-606.
5. Lund T., De Buyser M.L., Granum P.E. A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Mol Microbiol 2000, 38:254-261.
6. Fagerlund A., Ween O., Lund T., Hardy S.P., Granum P.E. Genetic and functional analysis of the cytK family of genes in Bacillus cereus. Microbiology 2004, 150:2689-2697.
7. Beecher D.J., Schoeni J.L., Wong A.C. Enterotoxic activity of hemolysin BL from Bacillus cereus. Infect Immun 1995, 63:4423-4428.
8. Lund T., Granum P.E. Characterisation of a non-haemolytic enterotoxin complex from Bacillus cereus isolated after a foodborne outbreak. FEMS Microbiol Lett 1996, 141:151-156.
9. Heinrichs J.H., Beecher D.J., MacMillan J.D., Zilinskas B.A. Molecular cloning and characterization of the hblA gene encoding the B component of hemolysin BL from Bacillus cereus. J Bacteriol 1993, 175:6760-6766.
10. Ryan P.A., Macmillan J.D., Zilinskas B.A. Molecular cloning and characterization of the genes encoding the L1 and L2 components of hemolysin BL from Bacillus cereus. J Bacteriol 1997, 179:2551-2556.
11. Granum P.E., O'Sullivan K., Lund T. The sequence of the non-haemolytic enterotoxin operon from Bacillus cereus. FEMS Microbiol Lett 1999, 177:225-229.
12. Agata N., Ohta M., Mori M., Isobe M. A novel dodecadepsipeptide, cereulide, is an emetic toxin of Bacillus cereus. FEMS Microbiol Lett 1995, 129:17-20.
13. Ehling-Schulz M., Fricker M., Scherer S. Identification of emetic toxin producing Bacillus cereus strains by a novel molecular assay. FEMS Microbiol Lett 2004, 232:189-195.
14. Ehling-Schulz M., Vukov N., Schulz A., Shaheen R., Andersson M., Märtlbauer E., et al. Identification and partial characterization of the nonribosomal peptide synthetase gene responsible for cereulide production in emetic Bacillus cereus. Appl Environ Microbiol 2005, 71:105-113.
15. Prüss B.M., Dietrich R., Nibler B., Märtlbauer E., Scherer S. The hemolytic enterotoxin HBL is broadly distributed among species of the Bacillus cereus group. Appl Environ Microbiol 1999, 65:5436-5442.
16. Moravek M., Dietrich R., Bürk C., Broussolle V., Guinebretiere M.H., Granum P.E., et al. Determination of the toxic potential of Bacillus cereus isolates by quantitative enterotoxin analyses. FEMS Microbiol Lett 2006, 257:293-298.
17. Yang I.C., Shih D.Y., Huang T.P., Huang Y.P., Wang J.Y., Pan T.M. Establishment of a novel multiplex PCR assay and detection of toxigenic strains of the species in the Bacillus cereus group. J Food Prot 2005, 68:2123-2130.
18. Ehling-Schulz M., Guinebretiere M.H., Monthan A., Berge O., Fricker M., Svensson B. Toxin gene profiling of enterotoxic and emetic Bacillus cereus. FEMS Microbiol Lett 2006, 260:232-240.
19. Ngamwongsatit P., Buasri W., Pianariyanon P., Pulsrikarn C., Ohba M., Assavanig A., et al. Broad distribution of enterotoxin genes (hblCDA, nheABC, cytK, and entFM) among Bacillus thuringiensis and Bacillus cereus as shown by novel primers. Int J Food Microbiol 2008, 121:352-356.
20. Wehrle E., Moravek M., Dietrich R., Bürk C., Didier A., Märtlbauer E. Comparison of multiplex PCR, enzyme immunoassay and cell culture methods for the detection of enterotoxinogenic Bacillus cereus. J Microbiol Meth 2009, 78:265-270.
21. Yang I.C., Shih D.Y., Wang J.Y., Pani T.M. Development of rapid real-time PCR and most-probable-number real-time PCR assays to quantify enterotoxigenic strains of the species in the Bacillus cereus group. J Food Prot 2007, 70:2774-2781.
22. Fricker M., Messelhäusser U., Busch U., Scherer S., Ehling-Schulz M. Diagnostic real-time PCR assays for the detection of emetic Bacillus cereus strains in foods and recent food-borne outbreaks. Appl Environ Microbiol 2007, 73:1892-1898.
23. Fan W., Hamilton T., Webster-Sesay S., Nikolich M.P., Lindler L.E. Multiplex real-time SYBR Green I PCR assay for detection of tetracycline efflux genes of Gram-negative bacteria. Mol Cell Probes 2007, 21:245-256.
24. Arya M., Shergill I.S., Williamson M., Gommersall L., Arya N., Patel H.R. Basic principles of real-time quantitative PCR. Expert Rev Mol Diagn 2005, 5:209-219.
25. Wittwer C.T., Herrmann M.G., Gundry C.N., Elenitoba-Johnson K.S. Real-time multiplex PCR assays. Methods 2001, 25:430-442.
26. Dietrich R., Fella C., Strich S., Märtlbauer E. Production and characterization of monoclonal antibodies against the hemolysin BL enterotoxin complex produced by Bacillus cereus. Appl Environ Microbiol 1999, 65:4470-4474.
27. Dietrich R., Moravek M., Bürk C., Granum P.E., Märtlbauer E. Production and characterization of antibodies against each of the three subunits of the Bacillus cereus nonhemolytic enterotoxin complex. Appl Environ Microbiol 2005, 71:8214-8220.
28. Ririe K.M., Rasmussen R.P., Wittwer C.T. Product differentiation by analysis of DNA melting curves during the polymerase chain reaction. Anal Biochem 1997, 245:154-160.
29. Walter M., Bonin M., Bauer P. LightCycler 480 system: high-throughput gene expression and genotyping analysis - a performance study. Biochemica 2006, 2:8-11.
30. Schoeni J.L., Wong A.C. Heterogeneity observed in the components of hemolysin BL, an enterotoxin produced by Bacillus cereus. Int J Food Microbiol 1999, 53:159-167.
31. Guinebretiere M.H., Broussolle V., Nguyen-The C. Enterotoxigenic profiles of food-poisoning and food-borne Bacillus cereus strains. J Clin Microbiol 2002, 40:3053-3056.
32. Thaenthanee S., Wong A.C.L., Panbangred W. Phenotypic and genotypic comparisons reveal a broad distribution and heterogeneity of hemolysin BL genes among Bacillus cereus isolates. Int J Food Microbiol 2005, 105:203-212.
33. Beattie S.H., Williams A.G. Detection of toxigenic strains of Bacillus cereus and other Bacillus spp. with an improved cytotoxicity assay. Lett Appl Microbiol 1999, 28:221-225.
34. Phelps R.J., McKillip J.L. Enterotoxin production in natural isolates of Bacillaceae outside the Bacillus cereus group. Appl Environ Microbiol 2002, 68:3147-3151.
35. Thorsen L., Hansen B.M., Nielsen K.F., Hendriksen N.B., Phipps R.K., Budde B.B. Characterization of emetic Bacillus weihenstephanensis, a new cereulide-producing bacterium. Appl Environ Microbiol 2006, 72:5118-5121.
36. McIntyre L., Bernard K., Beniac D., Isaac-Renton J.L., Naseby D.C. Identification of Bacillus cereus group species associated with food poisoning outbreaks in British Columbia, Canada. Appl Environ Microbiol 2008, 74:7451-7453.
37. Stenfors L.P., Mayr R., Scherer S., Granum P.E. Pathogenic potential of fifty B. weihenstephanensis strains. FEMS Microbiol Lett 2002, 215:47-51.
38. Altayar M., Sutherland A.D. Bacillus cereus is common in the environment but emetic toxin producing isolates are rare. J Appl Microbiol 2006, 100:7-14.
39. Kreuzberger C., Moravek M., Dietrich R., Scheurer R., Märtlbauer E. Characterisation of the toxicity of Bacillus cereus isolates from food supply facilities of the German Federal Armed Forces. Arch Lebensmittelhyg 2008, 59:92-98.
40. Fagerlund A., Brillard J., Fürst R., Guinebretriere M.H., Granumn P.E. Toxin production in a rare and genetically remote cluster of strains of the Bacillus cereus group. BMC Microbiol 2007, 7:43.
41. Ehling-Schulz M., Svensson B., Guinebretiere M.H., Lindback T., Andersson M., Schulz A., et al. Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains. Microbiology 2005, 151:183-197.
42. Fricker M., Messelhäusser U., Busch U., Scherer S., Ehling-Schulz M. Diagnostic Real-Time PCR assays for the detection of emetic Bacillus cereus strains in foods and recent food-borne outbreaks. Appl Environ Microbiol 2007, 73:1892-1898.
43. Martinez-Blanch J.F., Sanchez G., Garay E., Aznar R. Development of a real-time PCR assay for detection and quantification of enterotoxigenic members of Bacillus cereus group in food samples. Int J Food Microbiol 2009, 135:15-21.