Influence of curli expression by Escherichia coli O157:H7 on the cell's overall hydrophobicity, charge, and ability to attach to lettuce

Journal of Food Protection

Volumn 70, Issue 6, 2007, Pages 1339-1345

  Boyer, Renee R ^a   Sumner, Susan S ^a   Williams, Robert C ^a   Pierson, Merle D ^a   Popham, David L ^a   Kniel, Kalmia E ^b  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; LACTUCA;

EID: 34250304347     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-70.6.1339     Document Type: Article

References (46)

1. Arnqvist, A., A. Olsen, J. Pfeifer, D. G. Russell, and S. Normark. 1992. The Crl protein activates cryptic genes for curli formation and fibronectin binding in Escherichia coli HB101. Mol. Microbiol. 6: 2443-2452.
2. Benito, Y., C. Pin, M. Luisa Martin, M. Luisa Farcia, M. Delores Selagas, and C. Casas. 1997. Cell surface hydrophobicity and attachment of pathogenic and spoilage bacteria to meat surfaces. Meat Sci. 45:419-425.
3. Bougdour, A., C. Lelong, and J. Geiselmann. 2004. Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase sigma subunit of RNA polymerase. J. Biol. Chem. 279:19540-19550.
4. Briandet, R., T. Meylheuc, C. Maher, and M. N. Bellon-Fontaine. 1999. Listeria monocytogenes Scott A: cell surface charge, hydrophobicity, and electron donor and acceptor characteristics under different environmental growth conditions. Appl. Environ. Microbiol. 65:5328-5333.
5. Burnett, S. L., J. Chen, and L. R. Beuchat. 2000. Attachment of Escherichia coli O157:H7 to the surfaces and internal structures of apples as detected by confocal scanning laser microscopy. Appl. Environ. Microbiol. 66:4679-4687.
6. Castonguay, M. H., S. van der Schaaf, W. Koester, J. Krooneman, W. van der Meer, H. Harmsen, and P. Landini. 2006. Biofilm formation by Escherichia coli is stimulated by synergistic interactions and co-adhesion mechanisms with adherence-proficient bacteria. Res. Microbiol. 157:471-478.
7. Chapman, M. R., L. S. Robinson, J. S. Pinkner, R. Roth, J. Heuser, M. Hammar, S. Normark, and S. J. Hultgren. 2002. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851-855.
8. Collinson, S. K., S. C. Cloulhier, J. L. Doran, P. A. Banser, and W. W. Kay. 1996. Salmonella Enteritidis agfBAC operon encoding thin, aggregative fimbriae. J. Bacteriol. 178:662-667.
9. Cookson, A. L., W. A. Cooley, and M. J. Woodward. 2002. The role of type I and curli fimbriae of Shiga toxin-producing Escherichia coli in adherence to abiotic surfaces. Int. J. Med. Microbiol. 292: 195-205.
10. Dickson, J. S., and M. Koohmaraie. 1989. Cell surface charge characteristics and their relationship to bacterial attachment to meat surfaces. Appl. Environ. Microbiol. 55:832-836.
11. Fett, W. F. 1985. Relationship of bacterial cell surface hydrophobicity and charge to pathogenicity, physiologic race and immobilization in attached soybean leaves. Phytopathology 75:1414-1418.
12. Hassan, A. N., and J. F. Frank. 2004. Attachment of Escherichia coli O157:H7 grown in tryptic soy broth and nutrient broth to apple and lettuce surfaces as related to cell hydrophobicity, surface charge, and capsule production. Int. J. Food Microbiol. 96:103-109.
13. Jeter, C., and A. G. Matthysse. 2005. Characterization of the binding of diarrheagenic strains of E. coli to plant surfaces and the role of curli in the interaction of the bacteria with alfalfa sprouts. Mol. Plant Microbe Interact. 18:1235-1242.
14. Kim, S. H., and Y. H. Kim. 2004. Escherichia coli O157:H7 adherence to HEp-2 cells is implicated with curli expression and outer membrane integrity. J. Vet. Sci. 5:119-124.
15. Li, Y., and L. A. McLandsborough. 1999. The effects of the surface charge and hydrophobicity of Escherichia coli on its adhesion to beef muscle. Int. J. Food Microbiol. 53:193-195.
16. Lytle, D. A., E. W. Rice, C. H. Johnson, and K. R. Fox. 1999. Electrophoretic mobilities of Escherichia coli O157:H7 and wildtype Escherichia coli strains. Appl. Environ. Microbiol. 65:3222-3225.
17. Maurer, J. J., T. P. Brown, W. L. Steffens, and S. G. Thayer. 1998. The occurrence of ambient temperature-regulated adhesins, curli, and the temperature-sensitive hemagglutinin tsh among avian Escherichia coli. Avian Dis. 42:106-118.
18. Morris, C. E., J.-M. Monier, and M.-A. Jaques. 1997. Methods for observing microbial biofilms directly on leaf surfaces and recovering them for isolations of culturable microorganisms. Appl. Environ. Microbiol. 63:1570-1576.
19. Mozes, N., and P. G. Rouxhet. 1987. Methods for measuring hydrophobicity of microorganisms. J. Microbiol. Methods 6:99-112.
20. Olsen, A., A. Jonsson, and S. Normark. 1989. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338:652-655.
21. Pawar, D. M., M. L. Rossman, and J. Chen. 2005. Role of curli fimbriae in mediating the cells of enterohaemorrhagic Escherichia coli to attach to abiotic surfaces. J. Appl. Microbiol. 99:418-425.
22. Pederson, K. 1980. Electrostatic interaction chromatography, a method for assaying the relative surface charges of bacteria. FEMS Microbiol. Lett. 22:295-298
23. Prigent-Combaret, C., G. Prensier, T. T. Le Thi, O. Vidal, P. Lejeune, and C. Dorel. 2000. Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ. Microbiol. 2:450-464.
24. Provence, D. L., and R. Curtiss, 3rd. 1992. Role of crl in avian pathogenic Escherichia coli: a knockout mutation of crl does not affect hemagglutination activity, fibronectin binding, or curli production. Infect. Immun. 60:4460-4467.
25. Rangel, J. M., P. H. Sparling, C. Crowe, P. M. Griffin, and D. L. Swerdlow. 2005. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerg. Infect. Dis. 11:603-609.
26. Rivas, L., N. Fegan, and G. A. Dykes. 2005. Physicochemical properties of Shiga toxigenic Escherichia coli. J. Appl. Microbiol. 99: 716-727.
27. Romling, U., Z. Bian, M. Hammar, W. D. Sierralta, and S. Normark. 1998. Curli fibers are highly conserved between Salmonella Typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacterial. 180:722-731.
28. Rosenberg, M., D. Gutnick, and E. Rosenberg. 1980. Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol. Lett. 9:29-33.
29. Ryu, J. H., and L. R. Beuchat. 2005. Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Appl. Environ. Microbiol. 71:247-254.
30. Ryu, J. H., H. Kim, and L. R. Beuchat. 2004. Attachment and biofilm formation by Escherichia coli O157:H7 on stainless steel as influenced by exopolysaccharide production, nutrient availability, and temperature. J. Food Prot. 67:2123-2131.
31. Ryu, J. H., H. Kim, J. F. Frank, and L. R. Beuchat. 2004. Attachment and biofilm formation on stainless steel by Escherichia coli O157: H7 as affected by curli production. Lett. Appl. Microbiol. 39:359-362.
32. Seo, K. H., and J. F. Frank. 1999. Attachment of Escherichia coli O157:H7 to lettuce leaf surface and bacterial viability in response to chlorine treatment as demonstrated by using confocal scanning laser microscopy. J. Food Prot. 62:3-9.
33. Sherman, P., R. Soni, and M. Karmali. 1987. Surface properties of the vero cytotoxin-producing Escherichia coli O157:H7. Infect. Immun. 55:1824-1829.
34. Sukupolvi, S., R. G. Lorenz, J. I. Gordon, Z. Bian, J. D. Pfeifer, S. J. Normark, and M. Rhen. 1997. Expression of thin aggregative fimbriae promotes interaction of Salmonella Typhimurium SR-11 with mouse small intestinal epithelial cells. Infect. Immun. 65:5320-5325.
35. Takeuchi, K., and J. F. Frank. 2000. Penetration of Escherichia coli O157:H7 into lettuce tissues as affected by inoculum size and temperature and the effect of chlorine treatment on cell viability. J. Food Prot. 63:434-440.
36. 3. J. Food Prot. 64:1235-1239.
37. Takeuchi, K., and J. F. Frank. 2001. Quantitative determination of the role of lettuce leaf structures in protecting Escherichia coli O157: H7 from chlorine disinfection. J. Food Prot. 64:147-151.
38. Takeuchi, K., A. N. Hassan, and J. F. Frank. 2001. Penetration of Escherichia coli O157:H7 into lettuce as influenced by modified atmosphere and temperature. J. Food Prot. 64:1820-1823.
39. Takeuchi, K., C. M. Matute, A. N. Hassan, and J. F. Frank. 2000. Comparison of the attachment of Escherichia coli O157:H7, Listeria monocytogenes, Salmonella Typhimurium, and Pseudomonas fluorescens to lettuce leaves. J. Food Prot. 63:1433-1437.
40. Torres, A. G., C. Jeter, W. Langley, and A. G. Matthysse. 2005. Differential binding of Escherichia coli O157:H7 to alfalfa, human epithelial cells, and plastic is mediated by a variety of surface structures. Appl. Environ. Microbiol. 71:8008-8015.
41. Torres, A. G., and J. B. Kaper. 2003. Multiple elements controlling adherence of enterohemorrhagic Escherichia coli O157:H7 to HeLa cells. Infect. Immun. 71:4985-4995.
42. Uhlich, G. A., P. H. Cooke, and E. B. Solomon. 2006. Analyses of the red-dry-rough phenotype of an Escherichia coli O157:H7 strain and its role in biofilm formation and resistance to antibacterial agents. Appl. Environ. Microbiol. 72:2564-2572.
43. Uhlich, G. A., J. E. Keen, and R. O. Elder. 2001. Mutations in the csgD promoter associated with variations in curli expression in certain strains of Escherichia coli O157:H7. Appl. Environ. Microbiol. 67:2367-2370.
44. Uhlich, G. A., J. E. Keen, and R. O. Elder. 2002. Variations in the csgD promoter of Escherichia coli O157:H7 associated with increased virulence in mice and increased invasion of HEp-2 cells. Infect. Immun. 70:395-399.
45. Ukuku, D. O., and W. F. Fett. 2002. Relationship of cell surface charge and hydrophobicity to strength of attachment of bacteria to cantaloupe rind. J. Food Prot. 65:1093-1099.
46. Van Loosdrecht, C. M. M., J. Lyklema, W. Norde, G. Scharaa, and A. J. B. Zehnder. 1987. Electrophoretic mobility and hydrophobicity as a measure to predict the initial step of bacterial adhesion. Appl. Environ. Microbiol. 53:1898-1900.