Low concentrations of bile salts induce stress responses and reduce motility in Bacillus cereus ATCC 14570

Journal of Bacteriology

Volumn 189, Issue 14, 2007, Pages 5302-5313

  Kristoffersen, Simen M ^a   Ravnum, Solveig ^a   Tourasse, Nicolas J ^a   Økstad, Ole Andreas ^a   Kolstø, Anne Brit ^a   Davies, William ^a  

^a UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BILE SALT;

ARTICLE; BACILLUS CEREUS; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM ISOLATE; CELL MOTILITY; DNA MICROARRAY; DOWN REGULATION; EPIDEMIC; FOOD POISONING; NONHUMAN; PRIORITY JOURNAL; STRESS; UPREGULATION;

BACILLUS CEREUS; BILE ACIDS AND SALTS; CULTURE MEDIA; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTION, GENETIC;

BACILLUS CEREUS;

EID: 34447523988     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00239-07     Document Type: Article

References (75)

1. Agaisse, H., M. Gominet, O. A. Økstad, A. B. Kolstø, 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. Ohta, M. Mori, and M. Isobe. 1995. A novel dodecadepsipeptide, cereulide, is an emetic toxin of Bacillus cereus. FEMS Microbiol. Lett. 129:17-19.
3. Alekshun, M. N., and S. B. Levy. 1999. The mar regulon: multiple resistance to antibiotics and other toxic chemicals. Trends Microbiol. 7:410-413.
4. Alekshun, M. N., S. B. Levy, T. R. Mealy, B. A. Seaton, and J. F. Head. 2001. The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 angstrom resolution. Nat. Struct. Biol. 8:710-714.
5. Andersson, A., P. E. Granum, and U. Ronner. 1998. The adhesion of Bacillus cereus spores to epithelial cells might be an additional virulence mechanism. Int. J. Food Microbiol. 39:93-99.
6. Begley, M., C. G. M. Gahan, and C. Hill. 2002. Bile stress response in Listeria monocytogenes LO28: adaptation, cross-protection, and identification of genetic loci involved in bile resistance. Appl. Environ. Microbiol. 68:6005-6012.
7. Begley, M., C. G. M. Gahan, and C. Hill. 2005. The interaction between bacteria and bile. FEMS Microbiol. Rev. 29:625-651.
8. Bernstein, C., H. Bernstein, C. M. Payne, S. E. Beard, and J. Schneider. 1999. Bile salt activation of stress response promoters in Escherichia coli. Curr. Microbiol. 39:68-72.
9. Booth, I. R., and R. G. Kroll. 1983. Regulation of cytoplasmic Ph (Ph1) in bacteria and its relationship to metabolism. Biochem. Soc. Trans. 11:70-72.
10. Brillard, J., and D. Lereclus. 2004. Comparison of cytotoxin cytK promoters from Bacillus cereus strain ATCC 14579 and from a B. cereus food-poisoning strain. Microbiology 150:2699-2705.
11. Bron, P. A., M. Marco, S. M. Hoffer, E. Van Mullekom, W. M. de Vos, and M. Kleerebezem. 2004. Genetic characterization of the bile salt response in Lactobacillus plantarum and analysis of responsive promoters in vitro and in situ in the gastrointestinal tract. J. Bacteriol. 186:7829-7835.
12. Brown, M. H., and R. A. Skurray. 2001. Staphylococcal multidrug efflux protein QacA. J. Mol. Microbiol. Biotechnol. 3:163-170.
13. Browne, N., and B. C. A. Dowds. 2002. Acid stress in the food pathogen Bacillus cereus. J. Appl. Microbiol. 92:404-414.
14. Carey, M. C., and W. C. Duane. 1994. Enterohepatic circulation, p. 719-756. In I. M. Arias, J. l. Boyer, N. Fausto, W. B. Jackoby, D. A. Schachter, and D. A. Shafritz (ed.), The liver: biology and pathobiology, 3rd ed. Raven Press, Ltd., New York, NY.
15. Clavel, T., F. Carlin, D. Lairon, C. Nguyen-The, and P. Schmitt. 2004. Survival of Bacillus cereus spores and vegetative cells in acid media simulating human stomach. J. Appl. Microbiol. 97:214-219.
16. Cleveland, W. S., E. Grosse, and W. M. Shyu. 1991. Local regression models, p. 309-376. In J. M. Chambers and T. J. Hastie (ed.), Statistical models in S. Chapman & Hall, New York, NY.
17. Colmer, J. A., J. A. Fralick, and A. N. Hamood. 1998. Isolation and characterization of a putative multidrug resistance pump from Vibrio cholerae. Mol. Microbiol. 27:63-72.
18. Corning Life Sciences. 2005. UltraGAPS coated slides instruction manual. Corning Life Sciences, Corning, NY.
19. Dawson, P. A. 1998. Bile secretion and the enterohepatic circulation of bile acids, p. 1052-1063. In M. Feldman, M. H. Sleisenger, and B. F. Scharschmidt (ed.), Sleisenger and Fordtran's gastrointestinal and liver disease: pathophysiology/diagnosis/management, 6th ed. W. B. Saunders, Co., Philadelphia, PA.
20. de Jesus, M. C., A. A. Urban, M. E. Marasigan, and D. E. Barnett Foster. 2005. Acid and bile-salt stress of enteropathogenic Escherichia coli enhances adhesion to epithelial cells and alters glycolipid receptor binding specificity. J. Infect. Dis. 192:1430-1440.
21. Edwards, D. 2003. Non-linear normalization and background correction in one-channel cDNA microarray studies. Bioinformatics 19:825-833.
22. Fernandez Murga, M. L., D. Bernik, G. Font de Valdez, and A. E. Disalvo. 1999. Permeability and stability properties of membranes formed by lipids extracted from Lactobacillus acidophilus grown at different temperatures. Arch. Biochem. Biophys. 364:115-121.
23. Flahaut, S., J. Frere, P. Boutibonnes, and Y. Auffray. 1996. Comparison of the bile salts and sodium dodecyl sulfate stress responses in Enterococcus faecalis. Appl. Environ. Microbiol. 62:2416-2420.
24. Flahaut, S., A. Hartke, J. C. Giard, A. Benachour, P. Boutibonnes, and Y. Auffray. 1996. Relationship between stress response towards bile salts, acid and heat treatment in Enterococcus faecalis. FEMS Microbiol. Lett. 138:49-54.
25. Fujita, Y., T. Fujita, Y. Miwa, J. Nihashi, and Y. Aratani. 1986. Organization and transcription of the gluconate operon, gnt, of Bacillus subtilis. J. Biol. Chem. 261:13744-13753.
26. Gabriella, C., and S. M. Cutting. 2002. Bacillus probiotics: spore germination in the gastrointestinal tract. Appl. Environ. Microbiol. 68:2344-2352.
27. Gahan, C. G. M., J. O'Mahony, and C. Hill. 2001. Characterization of the groESL operon in Listeria monocytogenes: utilization of two reporter systems (gfp and hly) for evaluating in vivo expression. Infect. Immun. 69:3924-3932.
28. Gaillot, O., E. Pellegrini, S. Bregenholt, S. Nair, and P. Berche. 2000. The ClpP serine protease is essential for the intracellular parasitism and virulence of Listeria monocytogenes. Mol. Microbiol. 35:1286-1294.
29. Ghosh, A. C. 1978. Prevalence of Bacillus cereus in feces of healthy adults. J. Hyg. 80:233-236.
30. Gohar, M., O. A. Økstad, N. Gilois, V. Sanchis, A. B. Kolstø, and D. Lereclus. 2002. Two-dimensional electrophoresis analysis of the extracellular proteome of Bacillus cereus reveals the importance of the PlcR regulon. Proteomics 2:784-791.
31. Granum, P. E. 1994. Bacillus cereus and its toxins. J. Appl. Bacteriol. 76:S61-S66.
32. Granum, P. E., S. Brynestad, K. O'sullivan, and H. Nissen. 1993. Enterotoxin from Bacillus cereus - production and biochemical characterization. Neth. Milk Dairy J. 47:63-70.
33. Granum, P. E., and T. Lund. 1997. Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Lett. 157:223-228.
34. Haine, V., A. Sinon, F. Van Steen, S. Rousseau, M. Dozot, P. Lestrate, C. Lambert, J. J. Letesson, and X. De Bolle. 2005. Systematic targeted mutagenesis of Brucella melitensis 16M reveals a major role for GntR regulators in the control of virulence. Infect. Immun. 73:5578-5586.
35. Hardy, S. P., T. Lund, and P. E. Granum. 2001. CytK toxin of Bacillus cereus forms pores in planar lipid bilayers and is cytotoxic to intestinal epithelia. FEMS Microbiol. Lett. 197:47-51.
36. Hecker, M., and U. Völker. 2001. General stress repsonse of Bacillus subtilis and other bacteria. Adv. Microb. Physiol. 44:36-91.
37. Helgason, E., O. A. Økstad, D. A. Caugant, H. A. Johansen, A. Fouet, M. Mock, I. Hegna, and A. B. Kolstø. 2000. Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis - one species on the basis of genetic evidence. Appl. Environ. Microbiol. 66:2627-2630.
38. Hung, D. T., and J. J. Mekalanos. 2005. Bile acids induce cholera toxin expression in Vibrio cholerae in a ToxT-independent manner. Proc. Natl. Acad. Sci. USA 102:3028-3033.
39. Ivanova, N., A. Sorokin, I. Anderson, N. Galleron, B. Candelon, V. Kapatral, A. Bhattacharyya, G. Reznik, N. Mikhailova, A. Lapidus, L. Chu, M. Mazur, E. Goltsman, N. Larsen, M. D'Souza, T. Walunas, Y. Grechkin, G. Pusch, R. Haselkorn, M. Fonstein, S. D. Ehrlich, R. Overbeek, and N. Kyrpides. 2003. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423:87-91.
40. Kandell, R. L., and C. Bernstein. 1991. Bile-salt acid induction of DNA damage in bacterial and mammalian cells - implications for colon cancer. Nutr. Cancer 16:227-238.
41. Langlois, P., S. Bourassa, G. G. Poirier, and C. Beaulieu. 2003. Identification of Streptomyces coelicolor proteins that are differentially expressed in the presence of plant material. Appl. Environ. Microbiol. 69:1884-1889.
42. Le Breton, Y., A. Maze, A. Hartke, S. Lemarinier, Y. Auffray, and A. Rince. 2002. Isolation and characterization of bile salts-sensitive mutants of Enterococcus faecalis. Curr. Microbiol. 45:434-439.
43. Lechner, S., U. Muller-Ladner, K. Schlottmann, B. Jung, M. McClelland, J. Ruschoff, J. Welsh, J. Scholmerich, and F. Kullmann. 2002. Bile acids mimic oxidative stress induced upreguiation of thioredoxin reductase in colon cancer cell lines. Carcinogenesis 23:1281-1288.
44. Lereclus, D., H. Agaisse, M. Gominet, S. Salamitou, and V. Sanchis. 1996. Identification of a Bacillus thuringiensis gene that positively regulates transcription of the phosphatidylinositol-specific phospholipase C gene at the onset of the stationary phase. J. Bacteriol. 178:2749-2756.
45. Leverrier, P., D. Dimova, V. Pichereau, Y. Auffray, P. Boyaval, and G. L. Jan. 2003. Susceptibility and adaptive response to bile salts in Propionibacterium freudenreichii: physiological and proteomic analysis. Appl. Environ. Microbiol. 69:3809-3818.
46. Leverrier, P., J. P. C. Vissers, A. Rouault, P. Boyaval, and G. Jan. 2004. Mass spectrometry proteomic analysis of stress adaptation reveals both common and distinct response pathways in Propionibacterium freudenreichii. Arch. Microbiol. 181:215-230.
47. Lin, J., C. Cagliero, B. Guo, Y.-W. Barton, M.-C. Maurel, S. Payot, and Q. Zhang. 2005. Bile salts modulate expression of the CmeABC multidrug efflux pump in Campylobacter jejuni. J. Bacteriol. 187:7417-7424.
48. Lund, T., M. L. De Buyser, and P. E. Granum. 2000. A new cytotoxin from Bacillus cereus that may cause necrotic enteritis. Mol. Microbiol. 38:254-261.
49. Lund, T., and P. E. Granum. 1996. Characterisation of a non-haemolytic enterotoxin complex from Bacillus cereus isolated after a foodborne outbreak. FEMS Microbiol. Lett. 141:151-156.
50. Lund, T., and P. E. Granum. 1997. Comparison of biological effect of the two different enterotoxin complexes isolated from three different strains of Bacillus cereus. Microbiology 143:3329-3336.
51. Mei, J. M., F. Nourbakhsh, C. W. Ford, and D. W. Holden. 1997. Identification of Staphylococcus aureus virulence genes in a murine model of bacteraemia using signature-tagged mutagenesis. Mol. Microbiol. 26:399-407.
52. Melling, J., and B. J. Capel. 1978. Characteristics of Bacillus cereus emetic toxin. FEMS Microbiol. Lett. 4:133-135.
53. Periago, P. M., W. van Schaik, T. Abee, and J. A. Wouters. 2002. Identification of proteins involved in the heat stress response of Bacillus cereus ATCC 14579. Appl. Environ. Microbiol. 68:3486-3495.
54. Polissi, A., A. Pontiggia, G. Feger, M. Altieri, H. Mottl, L. Ferrari, and D. Simon. 1998. Large-scale identification of virulence genes from Streptococcus pneumoniae. Infect. Immun. 66:5620-5629.
55. Pope, L. M., K. E. Reed, and S. M. Payne. 1995. Increased protein secretion and adherence to HeLa cells by Shigella spp. following growth in the presence of bile salts. Infect. Immun. 63:3642-3648.
56. Prouty, A. M., I. E. Brodsky, J. Manos, R. Belas, S. Falkow, and J. S. Gunn. 2004. Transcriptional regulation of Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunol. Med. Microbiol. 41:177-185.
57. R Development Core Team. 2004. R: a language and environment for sta-tistical computing. R Foundation for Statistical Computing, Vienna, Austria.
58. Ramarao, N., and D. Lereclus. 2006. Adhesion and cytotoxicity of Bacillus cereus and Bacillus thuringiensis to epithelial cells are FlhA and PlcR dependent, respectively. Microbes Infect. 8:1483-1491.
59. Read, T. D., S. N. Peterson, N. Tourasse, L. W. Baillie, I. T. Paulsen, K. E. Nelson, H. Tettelin, D. E. Fouts, J. A. Eisen, S. R. Gill, E. K. Holtzapple, O. A. Økstad, E. Helgason, J. Rilstone, M. Wu, J. F. Kolonay, M. J. Beanan, R. J. Dodson, L. M. Brinkac, M. Gwinn, R. T. DeBoy, R. Madpu, S. C. Daugherty, A. S. Durkin, D. H. Haft, W. C. Nelson, J. D. Peterson, M. Pop, H. M. Khouri, D. Radune, J. L. Benton, Y. Mahamoud, L. Jiang, I. R. Hance, J. F. Weidman, K. J. Berry, R. D. Plaut, A. M. Wolf, K. L. Watkins, W. C. Nierman, A. Hazen, R. Cline, C. Redmond, J. E. Thwaite, O. White, S. L. Salzberg, B. Thomason, A. M. Friedlander, T. M. Koehler, P. C. Hanna, A. B. Kolstø, and C. M. Fraser. 2003. The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 423:81-86.
60. Read, T. D., S. L. Salzberg, M. Pop, M. Shumway, L. Umayam, L. Jiang, E. Holtzapple, J. D. Busch, K. L. Smith, J. M. Schupp, D. Solomon, P. Keim, and C. M. Fraser. 2002. Comparative genome sequencing for discovery of novel polymorphisms in Bacillus anthracis. Science 296:2028-2033.
61. Rince, A., S. Flahaut, and Y. Auffray. 2000. Identification of general stress genes in Enterococcus faecalis. Int. J. Food Microbiol. 55:87-91.
62. Sanchez, B., M. C. Champomier-Verges, P. Anglade, F. Baraige, C. G. de Los Reyes-Gavilan, A. Margolles, and M. Zagorec. 2005. Proteomic analysis of global changes in protein expression during bile salt exposure of Bifidobacterium longum NCIMB 8809. J. Bacteriol. 187:5799-5808.
63. Schmidt, G., and R. Zink. 2000. Basic features of the stress response in three species of Bifidobacteria: B. longum, B. adolescentis, and B. breve. Int. J. Food Microbiol. 55:41-45.
64. Smyth, G. K. 2005. Limma: linear models for microarray data, p. 397-420. In R. Gentleman, V. Carey, S. Dudoit, R. Irizarry, and W. Huber (ed.), Bioinformatics and computational biology solutions using R and bioconductor. Springer, New York, NY.
65. Sokol, R. J., B. M. Winklhoferroob, M. W. Devereaux, and J. M. McKim. 1995. Generation of hydroperoxides in isolated rat hepatocytes and hepatic mitochondria exposed to hydrophobic bile-acids. Gastroenterology 109:1249-1256.
66. Tam, N. K., N. Q. Uyen, H. A. Hong, H. Due le, T. T. Hoa, C. R. Serra, A. O. Henriques, and S. M. Cutting. 2006. The intestinal life cycle of Bacillus subtilis and close relatives. J. Bacteriol. 188:2692- 2700.
67. Taranto, M. P., M. L. F. Murga, G. Lorca, and G. F. de Valdez. 2003. Bile salts and cholesterol induce changes in the lipid cell membrane of Lactobacillus reuteri. J. Appl. Microbiol. 95:86-91.
68. Tatusov, R. L., E. V. Koonin, and D. J. Lipman. 1997. A genomic perspective on protein families. Science 278:631-637.
69. Taylor, D. E. 1999. Bacterial tellurite resistance. Trends Microbiol. 7:111-115.
70. Turnbull, P. C. B., R. A. Hutson, M. J. Ward, M. N. Jones, C. P. Quinn, N. J. Finnie, C. J. Duggleby, J. M. Kramer, and J. Melling. 1992. Bacillus anthracis but not always anthrax. J. Appl. Bacteriol. 72:21-28.
71. B of Bacillus cereus: response to stress and role in heat adaptation. J. Bacteriol. 186:316-325.
72. B-dependent genes in Bacillus cereus by proteome and in vitro transcription analysis. J. Bacteriol. 186:4100-4109.
73. Wijnands, L. M., J. B. Dufrenne, M. H. Zwietering, and F. M. van Leusden. 2006. Spores from mesophilic Bacillus cereus strains germinate better and grow faster in simulated gastro-intestinal conditions than spores from psychrotrophic strains. Int. J. Food Microbiol. 112:120-128.
74. Wilcks, A., B. M. Hansen, N. B. Hendriksen, and T. R. Licht. 2006. Fate and effect of ingested Bacillus cereus spores and vegetative cells in the intestinal tract of human-flora-associated rats. FEMS Immunol. Med. Microbiol. 46:70-77.
75. Xu, Y., R. J. Heath, Z. Li, C. O. Rock, and S. W. White. 2001. The FadR-DNA complex. Transcriptional control of fatty acid metabolism in Escherichia coli. J. Biol. Chem. 276:17373-17379.