Identification of the main promoter directing cereulide biosynthesis in emetic bacillus cereus and its application for real-time monitoring of ees gene expression in foods

Applied and Environmental Microbiology

Volumn 76, Issue 4, 2010, Pages 1232-1240

  Dommel, Monica K ^a   Frenzel, Elrike ^a   Strasser, Bernd ^a   Blöchinger, Claudia ^a   Scherer, Siegfried ^a   Ehling Schulz, Monika ^b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL CHARACTERIZATION; BIOMONITORING; CDNA ENDS; CODING SEQUENCES; COMPLEX ENVIRONMENTS; COMPLEX MATRICES; DELETION ANALYSIS; FOOD MATRIXES; HYDROLASES; LUCIFERASE GENES; NONRIBOSOMAL PEPTIDE SYNTHETASES; ORDERS OF MAGNITUDE; PRIMER EXTENSION; PROMOTER ACTIVITIES; PROMOTER ELEMENTS; PROMOTER REGION; REAL TIME MONITORING; REFERENCE STRAINS; REPORTER SYSTEMS; STRUCTURAL ORGANIZATION; SYNTHETASES; TRANSCRIPTION INITIATION;

AMPLIFICATION; BACILLUS CEREUS; BACTERIOLOGY; BIOACTIVITY; BIOCHEMISTRY; ENCODING (SYMBOLS); GENE ENCODING;

TRANSCRIPTION;

BACTERIAL DNA; BACTERIAL TOXIN; CEREULIDE; DEPSIPEPTIDE; NON RIBOSOMAL PEPTIDE SYNTHASE; NON-RIBOSOMAL PEPTIDE SYNTHASE; PEPTIDE SYNTHASE; PRIMER DNA;

BACTERIUM; BIOMONITORING; DNA; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENETIC ANALYSIS; REAL TIME;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS CEREUS; BACTERIAL GENE; BIOSYNTHESIS; ENVIRONMENTAL MONITORING; FOOD CONTROL; FOOD POISONING; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PROMOTER REGION; REPORTER GENE; VOMITING;

AMINO ACID SEQUENCE; BACILLUS CEREUS; BACTERIAL TOXINS; BASE SEQUENCE; DEPSIPEPTIDES; DNA PRIMERS; DNA, BACTERIAL; ENVIRONMENTAL MONITORING; FOOD MICROBIOLOGY; FOODBORNE DISEASES; GENE EXPRESSION; GENES, BACTERIAL; GENES, REPORTER; HUMANS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PEPTIDE SYNTHASES; PROMOTER REGIONS, GENETIC; VOMITING;

BACILLUS CEREUS;

EID: 76649087644     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02317-09     Document Type: Article

References (64)

1. Agaisse, H., M. Gominet, O. A. Okstad, A.-B. Kolsto, and D. Lereclus. 1999. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol. Microbiol. 32: 1043-1053.
2. Agata, N., M. Mori, M. Ohta, S. Suwan, I. Ohtani, and M. Isobe. 1994. A novel dodecadepsipeptide, cereulide, isolated from Bacillus cereus causes vacuole formation in HEp-2 cells. FEMS Microbiol. Lett. 121: 31-34.
3. Agata, N., M. Ohta, and K. Yokoyama. 2002. Production of Bacillus cereus emetic toxin (cereulide) in various foods. Int. J. Food Microbiol. 73: 23-27.
4. Beecher, D. J., and J. D. Macmillan. 1991. Characterization of the components of hemolysin BL from Bacillus cereus. Infect. Immun. 59: 1778-1784.
5. Bertani, G. 1951. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62: 293-300.
6. 6. Borchert, S., T. Stachelhaus, and M. Marahiel. 1994. Induction of surfactin production in Bacillus subtilis by gsp, a gene located upstream of the gramicidin S operon in Bacillus brevis. J. Bacteriol. 176: 2458-2462. (Pubitemid 24118201)
7. Brendel, V., and E. N. Trifonov. 1984. A computer algorithm for testing potential prokaryotic terminators. Nucleic Acids Res. 12: 4411-4427.
8. Bresolin, G., K. Neuhaus, S. Scherer, and T. M. Fuchs. 2006. Transcriptional analysis of long-term adaptation of Yersinia enterocolitica to low-temperature growth. J. Bacteriol. 188: 2945-2958.
9. Caboche, S., M. Pupin, V. Leclere, A. Fontaine, P. Jacques, and G. Kucherov. 2008. NORINE: a database of nonribosomal peptides. Nucleic Acids Res. 36: D326-D331.
10. Callegan, M. C., S. T. Kane, D. C. Cochran, B. Novosad, M. S. Gilmore, M. Gominet, and D. Lereclus. 2005. Bacillus endophthalmitis: roles of bacterial toxins and motility during infection. Invest. Ophthalmol. Vis. Sci. 46: 3233-3238.
11. 11. Cormack, B. P., R. H. Valdivia, and S. Falkow. 1996. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173: 33-38. (Pubitemid 26239677)
12. 12. Cosmina, P., F. Rodriguez, F. de Ferra, G. Grandi, M. Perego, G. Venema, and D. van Sinderen. 1993. Sequence and analysis of the genetic locus responsible for surfactin synthesis in Bacillus subtilis. Mol. Microbiol. 8: 821-831. (Pubitemid 23171464)
13. Crosa, J. H., and C. T. Walsh. 2002. Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol. Mol. Biol. Rev. 66: 223-249.
14. Dierick, K., E. Van Coillie, I. Swiecicka, G. Meyfroidt, H. Devlieger, A. Meulemans, G. Hoedemaekers, L. Fourie, M. Heyndrickx, and J. Mahillon. 2005. Fatal family outbreak of Bacillus cereus-associated food poisoning. J. Clin. Microbiol. 43: 4277-4279.
15. Dunn, A. K., and J. Handelsman. 1999. A vector for promoter trapping in Bacillus cereus. Gene 226: 297-305.
16. Duport, C., A. Zigha, E. Rosenfeld, and P. Schmitt. 2006. Control of enterotoxin gene expression in Bacillus cereus F4430/73 involves the redox-sensitive ResDE signal transduction system. J. Bacteriol. 188: 6640-6651.
17. Ehling-Schulz, M., M. Fricker, H. Grallert, P. Rieck, M. Wagner, and S. Scherer. 2006. Cereulide synthetase gene cluster from emetic Bacillus cereus: structure and location on a mega virulence plasmid related to Bacillus anthracis toxin plasmid pXO1. BMC Microbiol. 6:20.
18. Ehling-Schulz, M., M. Fricker, and S. Scherer. 2004. Bacillus cereus, the causative agent of an emetic type of food-borne illness. Mol. Nutr. Food Res. 48: 479-487.
19. Ehling-Schulz, M., M. Fricker, and S. Scherer. 2004. Identification of emetic toxin producing Bacillus cereus strains by a novel molecular assay. FEMS Microbiol. Lett. 232: 189-195.
20. Ehling-Schulz, M., B. Svensson, M.-H. Guinebretiere, T. Lindback, M. Andersson, A. Schulz, M. Fricker, A. Christiansson, P. E. Granum, E. Martlbauer, C. Nguyen-The, M. Salkinoja-Salonen, and S. Scherer. 2005. Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains. Microbiology 151: 183-197.
21. 21. Ehling-Schulz, M., N. Vukov, A. Schulz, R. Shaheen, M. Andersson, E. Martlbauer, and S. Scherer. 2005. Identification and partial characterization of the nonribosomal peptide synthetase gene responsible for cereulide production in emetic Bacillus cereus. Appl. Environ. Microbiol. 71: 105-113. (Pubitemid 40116257)
22. Fagerlund, A., O. Ween, T. Lund, S. P. Hardy, and P. E. Granum. 2004. Genetic and functional analysis of the cytK family of genes in Bacillus cereus. Microbiology 150: 2689-2697.
23. Farabaugh, P. J. 1996. Programmed translational frameshifting. Annu. Rev. Genet. 30: 507-528.
24. Finking, R., and M. A. Marahiel. 2004. Biosynthesis of nonribosomal peptides. Annu. Rev. Microbiol. 58: 453-488.
25. Finlay, W. J., N. A. Logan, and A. D. Sutherland. 2002. Bacillus cereus emetic toxin production in cooked rice. Food Microbiol. 19: 431-439.
26. Finlay, W. J., N. A. Logan, and A. D. Sutherland. 1999. Semiautomated metabolic staining assay for Bacillus cereus emetic toxin. Appl. Environ. Microbiol. 65: 1811-1812.
27. Francis, K. P., D. Joh, C. Bellinger-Kawahara, M. J. Hawkinson, T. F. Purchio, and P. R Contag. 2000. Monitoring bioluminescent Staphylococcus aureus infections in living mice using a novel luxABCDE construct. Infect. Immun. 68: 3594-3600.
28. Fricker, M., U. Messelhausser, U. Busch, S. Scherer, and M. Ehling-Schulz. 2007. Diagnostic real-time PCR assays for the detection of emetic Bacillus cereus strains in foods and recent food-borne outbreaks. Appl. Environ. Microbiol. 73: 1892-1898.
29. Gohar, M., K. Faegri, S. Perchat, S. Ravnum, O. A. Okstad, M. Gominet, A. B. Kolsto, and D. Lereclus. 2008. The PlcR virulence regulon of Bacillus cereus. PLoS One 3: e2793.
30. Granum, P. E., K. O'Sullivan, and T. Lund. 1999. The sequence of the non-haemolytic enterotoxin operon from Bacillus cereus. FEMS Microbiol. Lett. 177: 225-229.
31. Häggblom, M. M., C. Apetroaie, M. A. Andersson, and M. S. SalkinojaSalonen. 2002. Quantitative analysis of cereulide, the emetic toxin of Bacillus cereus, produced under various conditions. Appl. Environ. Microbiol. 68: 2479-2483.
32. Ishii, T., K.-I. Yoshida, G. Terai, Y. Fujita, and K. Nakai. 2001. DBTBS: a database of Bacillus subtilis promoters and transcription factors. Nucleic Acids Res. 29: 278-280.
33. Jääskeläinen, E. L., V. Teplova, M. A. Andersson, L. C. Andersson, P. Tammela, M. C. Andersson, T. I. Pirhonen, N.-E. L. Saris, P. Vuorela, and M. S. Salkinoja-Salonen. 2003. In vitro assay for human toxicity of cereulide, the emetic mitochondrial toxin produced by food poisoning Bacillus cereus. Toxicol. In Vitro 17: 737-744.
34. Kaebernick, M., E. Dittmann, T. Borner, and B. A. Neilan. 2002. Multiple alternate transcripts direct the biosynthesis of microcystin, a cyanobacterial nonribosomal peptide. Appl. Environ. Microbiol. 68: 449-455.
35. Kramer, J. M., and R. J. Gilbert. 1989. Bacillus cereus and other Bacillus species, p. 21-70. In M. P. Doyle (ed.), Food-borne bacterial pathogens. Marcel Dekker, New York, NY.
36. Krätzschmar, J., M. Krause, and M. A. Marahiel. 1989. Gramicidin S biosynthesis operon containing the structural genes grsA and grsB has an open reading frame encoding a protein homologous to fatty acid thioesterases. J. Bacteriol. 171: 5422-5429.
37. Logemann, J., J. Schell, and L. Willmitzer. 1987. Improved method for the isolation of RNA from plant tissues. Anal. Biochem. 163: 16-20.
38. Lucking, G., M. K. Dommel, S. Scherer, A. Fouet, and M. Ehling-Schulz. 2009. Cereulide synthesis in emetic Bacillus cereus is controlled by the transition state regulator AbrB, but not by the virulence regulator PlcR. Microbiology 155: 922-931.
39. Lund, T., M. De Buyser, and P. Granum. 2000. A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Mol. Microbiol. 38: 254-261.
40. Magarvey, N. A., M. Ehling-Schulz, and C. T. Walsh. 2006. Characterization of the cereulide NRPS hydroxy acid specifying modules: activation of keto acids and chiral reduction on the assembly line. J. Am. Chem. Soc. 128: 10698-10699.
41. Mahler, H., A. Pasi, J. M. Kramer, P. Schulte, A. C. Scoging, W. Bar, and S. Krahenbuhl. 1997. Fulminant liver failure in association with the emetic toxin of Bacillus cereus. N. Engl. J. Med. 336: 1142-1148.
42. Marahiel, M. A., T. Stachelhaus, and H. D. Mootz. 1997. Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem. Rev. 97: 2651-2674.
43. Martineau, F., F. J. Picard, P. H. Roy, M. Ouellette, and M. G. Bergeron. 1996. Species-specific and ubiquitous DNA-based assays for rapid identification of Staphylococcus epidermidis. J. Clin. Microbiol. 34: 2888-2893.
44. 44. Moon, S., Y. Byun, H.-J. Kim, S. Jeong, and K. Han. 2004. Predicting genes expressed via -1 and +1 frameshifts. Nucleic Acids Res. 32: 4884-4892. (Pubitemid 39429692)
45. Okstad, O. A., M. Gominet, B. Purnelle, M. Rose, D. Lereclus, and A.-B. Kolsto. 1999. Sequence analysis of three Bacillus cereus loci carrying PIcRregulated genes encoding degradative enzymes and enterotoxin. Microbiology 145: 3129-3138.
46. Ouhib, O., T. Clavel, and P. Schmitt. 2006. The production of Bacillus cereus enterotoxins is influenced by carbohydrate and growth rate. Curr. Microbiol. 53: 222-226.
47. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29: e45.
48. Pósfay-Barbe, K. M., J. Schrenzel, J. Frey, R. Studer, C. Korff, D. C. Belli, P. Parvex, P. C. Rimensberger, and M. G. Schappi. 2008. Food poisoning as a cause of acute liver failure. Pediatr. Infect. Dis. J. 27: 846-847.
49. Rajkovic, A., M. Uyttendaele, and J. Debevere. 2007. Computer aided boar semen motility analysis for cereulide detection in different food matrices. Int. J. Food Microbiol. 114: 92-99.
50. Rajkovic, A., M. Uyttendaele, W. Deley, A. Van Soom, T. Rijsselaere, and J. Debevere. 2006. Dynamics of boar semen motility inhibition as a semiquantitative measurement of Bacillus cereus emetic toxin (cereulide). J. Microbiol. Methods 65: 525-534.
51. Rajkovic, A., M. Uyttendaele, A. Vermeulen, M. Andjelkovic, I. FitzJames, P. in 't Veld, Q. Denon, R. Verhe, and J. Debevere. 2008. Heat resistance of Bacillus cereus emetic toxin, cereulide. Lett. Appl. Microbiol. 46: 536-541.
52. Rasko, D. A., M. J. Rosovitz, O. A. Okstad, D. E. Fouts, L. Jiang, R. Z. Cer, A.-B. Kolsto, S. R Gill, and J. Ravel. 2007. 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 B. anthracis pXO1. J. Bacteriol. 189: 52-64.
53. Reese, M. G. 2001. Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comp. Chem. 26: 51-56.
54. Schoeni, J. L., and A. C. L. Wong. 2005. Bacillus cereus food poisoning and its toxins. J. Food Prot. 68: 636-648.
55. Shaheen, R., M. A. Andersson, C. Apetroaie, A. Schulz, M. Ehling-Schulz, V. M. Ollilainen, and M. S. Salkinoja-Salonen. 2006. Potential of selected infant food formulas for production of Bacillus cereus emetic toxin, cereulide. Int. J. Food Microbiol. 107: 287-294.
56. Shinagawa, K., H. Konuma, H. Sekita, and S. Sugii. 1995. Emesis of rhesus monkeys induced by intragastric administration with the HEp-2 vacuolation factor (cereulide) produced by Bacillus cereus. FEMS Microbiol. Lett. 130: 87-90.
57. Sieber, S. A., and M. A. Marahiel. 2005. Molecular mechanisms underlying nonribosomal peptide synthesis: approaches to new antibiotics. Chem. Rev. 105: 715-738.
58. Stenfors Arnesen, L. P., A. Fagerlund, and P. E. Granum. 2008. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Rev. 32: 579-606.
59. Szabo, R., J. Speirs, and M. Akhtar. 1991. Cell culture detection and conditions for production of a Bacillus cereus heat-stable toxin. J. Food Prot. 54: 272-276.
60. Thorsen, L., B. M. Hansen, K. F. Nielsen, N. B. Hendriksen, R. K. Phipps, and B. B. Budde. 2006. Characterization of emetic Bacillus weihenstephanensis, a new cereulide-producing bacterium. Appl. Environ. Microbiol. 72: 5118-5121.
61. Turnbull, P. C., J. M. Kramer, K. Jorgensen, R. J. Gilbert, and J. Melling. 1979. Properties and production characteristics of vomiting, diarrheal, and necrotizing toxins of Bacillus cereus. Am. J. Clin. Nutr. 32: 219-228.
62. Vassileva, M., K. Torii, M. Oshimoto, A. Okamoto, N. Agata, K. Yamada, T. Hasegawa, and M. Ohta. 2007. A new phylogenetic cluster of cereulide-producing Bacillus cereus strains. J. Clin. Microbiol. 45: 1274-1277.
63. Wang, N., S.-E. Lu, Q. Yang, S.-H. Sze, and D. C. Gross. 2006. Identification of the syr-syp box in the promoter regions of genes dedicated to syringomycin and syringopeptin production by Pseudomonas syringae pv. syringae B301D. J. Bacteriol. 188: 160-168.
64. Zuker, M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31: 3406-3415.