EhaA is a novel autotransporter protein of enterohemorrhagic Escherichia coli O157:H7 that contributes to adhesion and biofilm formation

Environmental Microbiology

Volumn 10, Issue 3, 2008, Pages 589-604

  Wells, Timothy J ^a   Sherlock, Orla ^a   Rivas, Lucy ^b   Mahajan, Arvind ^c   Beatson, Scott A ^a   Torpdahl, Mia ^d   Webb, Richard I ^a   Allsopp, Luke P ^a   Gobius, Kari S ^b   Gally, David L ^c   Schembri, Mark A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b CSIRO   (Australia)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d STATENS SERUM INSTITUT   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; EHAA, ESCHERICHIA COLI O157:H7; ESCHERICHIA COLI PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM ADHERENCE; BIOFILM; CHEMISTRY; ESCHERICHIA COLI O157; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ADHESINS, ESCHERICHIA COLI; BACTERIAL ADHESION; BIOFILMS; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS); BOVINAE; ESCHERICHIA COLI; ESCHERICHIA COLI K12; NEGIBACTERIA;

EID: 38549133764     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2007.01479.x     Document Type: Article

References (64)

1. Bachmann, B. (1996) Derivations and genotypes of some mutant derivatives of Escherichia coli K-12. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed. Neidhardt, F.C., Curtiss, R. III., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik B., et al. (eds). Washington, DC, USA : American Society for Microbiology, 2460 2488.
2. Bakker, D., Willemsen, P.T.J., Simons, L.H., Vanzijderveld, F.G. Degraaf, F.K. (1992) Characterization of the antigenic and adhesive properties of faeg, the major subunit of K88 fimbriae. Mol Microbiol 6 : 247 255.
3. Bendtsen, J.D., Nielsen, H., von Heijne, G. Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 : 783 795.
4. Borczyk, A.A., Karmali, M.A., Lior, H. Duncan, L.M. (1987) Bovine reservoir for verotoxin-producing Escherichia coli O157: H7. Lancet 1 : 98.
5. Christensen, B.B., Sternberg, C., Andersen, J.B., Palmer, R.J. Jr, Nielsen, A.T., Givskov, M. Molin, S. (1999) Molecular tools for study of biofilm physiology. Methods Enzymol 310 : 20 42.
6. Cornick, N.A., Booher, S.L. Moon, H.W. (2002) Intimin facilitates colonization by Escherichia coli O157:H7 in adult ruminants. Infect Immun 70 : 2704 2707.
7. Costerton, J.W., Stewart, P.S. Greenberg, E.P. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284 : 1318 1322.
8. Datsenko, K.A. Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97 : 6640 6645.
9. Dean-Nystrom, E.A., Bosworth, B.T., Cray, W.C. Moon, H.W. (1997) Pathogenicity of Escherichia coli O157:H7 in the intestines of neonatal calves. Infect Immun 65 : 1842 1848.
10. Dean-Nystrom, E.A., Bosworth, B.T., Moon, H.W. O'Brien, A.D. (1998) Escherichia coli O157:H7 requires intimin for enteropathogenicity in calves. Infect Immun 66 : 4560 4563.
11. Dean-Nystrom, E.A., Pohlenz, J.F., Moon, H.W. O'Brien, A.D. (2000) Escherichia coli O157:H7 causes more-severe systemic disease in suckling piglets than in colostrum-deprived neonatal piglets. Infect Immun 68 : 2356 2358.
12. Desvaux, M., Parham, N.J. Henderson, I.R. (2004) The autotransporter secretion system. Res Microbiology 155 : 53 60.
13. Dziva, F., van Diemen, P.M., Stevens, M.P., Smith, A.J. Wallis, T.S. (2004) Identification of Escherichia coli O157:H7 genes influencing colonization of the bovine gastrointestinal tract using signature-tagged mutagenesis. Microbiology 150 : 3631 3645.
14. Dziva, F., Mahajan, A., Cameron, P., Currie, C., McKendrick, I.J., Wallis, T.S., et al. (2007) EspP, a type V-secreted serine protease of enterohaemorrhagic Escherichia coli O157: H7, influences intestinal colonization of calves and adherence to bovine primary intestinal epithelial cells. FEMS Microbiol Lett 271 : 258 264.
15. Frankel, G., Phillips, A.D., Rosenshine, I., Dougan, G., Kaper, J.B. Knutton, S. (1998) Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol Microbiol 30 : 911 921.
16. Guzman, L.M., Belin, D., Carson, M.J. Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose pBAD promoter. J Bacteriol 177 : 4121 4130.
17. Hasman, H., Chakraborty, T. Klemm, P. (1999) Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J Bacteriol 181 : 4834 4841.
18. Henderson, I.R. Nataro, J.P. (2001) Virulence functions of autotransporter proteins. Infect Immun 69 : 1231 1243.
19. Henderson, I.R., Navarro-Garcia, F. Nataro, J.P. (1998) The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6 : 370 378.
20. Henderson, I.R., Navarro-Garcia, F., Desvaux, M., Fernandez, R.C. Ala'Aldeen, D. (2004) Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68 : 692 744.
21. Hoey, D.E.E., Sharp, L., Currie, C., Lingwood, C.A., Gally, D.L. Smith, D.G.E. (2003) Verotoxin 1 binding to intestinal crypt epithelial cells results in localization to lysosomes and abrogation of toxicity. Cell Microbiol 5 : 85 97.
22. Kjaergaard, K., Schembri, M.A., Ramos, C., Molin, S. Klemm, P. (2000) Antigen 43 facilitates formation of multispecies biofilms. Environ Microbiol 2 : 695 702.
23. Klemm, P., Hjerrild, L., Gjermansen, M. Schembri, M.A. (2004) Structure-function analysis of the self-recognizing Antigen 43 autotransporter protein from Escherichia coli. Mol Microbiol 51 : 283 296.
24. Kresse, A.U., Schulze, K., Deibel, C., Ebel, F., Rohde, M., Chakraborty, T. Guzman, C.A. (1998) Pas, a novel protein required for protein secretion and attaching and effacing activities of enterohemorrhagic Escherichia coli. J Bacteriol 180 : 4370 4379.
25. Lam, J.S. Mutharia, L.M. (1994) Antigen-antibody reactions. In Methods for General and Molecular Bacteriology. Gerhardt, P. (ed.). Washington, DC, USA : ASM, pp. 104 132.
26. Louie, M., Read, S., Louie, L., Ziebell, K., Rahn, K., Borczyk, A. Lior, H. (1999) Molecular typing methods to investigate transmission of Escherichia coli O157:H7 from cattle to humans. Epidemiol Infect 123 : 17 24.
27. Low, J.C., McKendrick, I.J., McKechnie, C., Fenlon, D., Naylor, S.W., Currie, C., et al. (2005) Rectal carriage of enterohemorrhagic Escherichia coli O157 in slaughtered cattle. Appl Environ Microbiol 71 : 93 97.
28. Low, A.S., Dziva, F., Torres, A.G., Martinez, J.L., Rosser, T., Naylor, S., et al. (2006) Cloning, expression, and characterization of fimbrial operon F9 from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 74 : 2233 2244.
29. McCullagh, P.A.N. J.A. (1989) Generalized Linear Models. London, UK : Chapman & Hall.
30. McDaniel, T.K., Jarvis, K.G., Donnenberg, M.S. Kaper, J.B. (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92 : 1664 1668.
31. Maki, D.G. (2006) Don't eat the spinach - controlling foodborne infectious disease. N Engl J Med 355 : 1952 1955.
32. Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., et al. (1999) Food-related illness and death in the United States. Emerg Infect Dis 5 : 607 625.
33. Melton-Celsa, A.R., Smith, M.J. O'Brien, A.D. (2005) Shiga toxins: potent poisons, pathogenicity determinants, and pharmacological agents. In EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology. Curtiss, R. III (ed. in Chief). Washington, DC, USA : ASMPress. [WWW document]. URL http://www.ecosal.org. Module. 8.7.8.
34. Michino, H., Araki, K., Minami, S., Takaya, S., Sakai, N., Miyazaki, M., et al. (1999) Massive outbreak of Escherichia coli O157:H7 infection in schoolchildren in Sakai City, Japan, associated with consumption of white radish sprouts. Am J Epidemiol 150 : 787 796.
35. Nataro, J.P. Kaper, J.B. (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11 : 142 201.
36. Naylor, S.W., Low, J.C., Besser, T.E., Mahajan, A., Gunn, G.J., Pearce, M.C., et al. (2003) Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infect Immun 71 : 1505 1512.
37. Naylor, S.W., Roe, A.J., Nart, P., Spears, K., Smith, D.G., Low, J.C. Gally, D.L. (2005) Escherichia coli O157:H7 forms attaching and effacing lesions at the terminal rectum of cattle and colonization requires the LEE4 operon. Microbiology 151 : 2773 2781.
38. Pawar, D.M., Rossman, M.L. Chen, J. (2005) Role of curli fimbriae in mediating the cells of enterohaemorrhagic Escherichia coli to attach to abiotic surfaces. J Appl Microbiol 99 : 418 425.
39. Perna, N.T., Plunkett, G., 3rd, Burland, V., Mau, B., Glasner, J.D., Rose, D.J., et al. (2001) Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409 : 529 533.
40. Rangel, J.M., Sparling, P.H., Crowe, C., Griffin, P.M. Swerdlow, D.L. (2005) Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerg Infect Dis 11 : 603 609.
41. Reisner, A., Molin, S. Zechner, E.L. (2002) Recombinogenic engineering of conjugative plasmids with fluorescent marker cassettes. FEMS Microbiol Ecol 42 : 251 259.
42. Reisner, A., Haagensen, J.A., Schembri, M.A., Zechner, E.L. Molin, S. (2003) Development and maturation of Escherichia coli K-12 biofilms. Mol Microbiol 48 : 933 946.
43. Roe, A.J., Currie, C., Smith, D.G. Gally, D.L. (2001) Analysis of type 1 fimbriae expression in verotoxigenic Escherichia coli: a comparison between serotypes O157 and O26. Microbiology 147 : 145 152.
44. Roux, A., Beloin, C. Ghigo, J.M. (2005) Combined inactivation and expression strategy to study gene function under physiological conditions: application to identification of new Escherichia coli adhesins. J Bacteriol 187 : 1001 1013.
45. Ryu, J.H. Beuchat, L.R. (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.
46. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, New York, USA : Cold Spring Harbor Laboratory Press.
47. Schembri, M.A. Klemm, P. (2001) Biofilm formation in a hydrodynamic environment by novel FimH variants and ramifications for virulence. Infect Immun 69 : 1322 1328.
48. Schembri, M.A., Givskov, M. Klemm, P. (2002) An attractive surface: gram-negative bacterial biofilms. Sci STKE 2002 : RE6.
49. Schembri, M.A., Dalsgaard, D. Klemm, P. (2004a) Capsule shields the function of short bacterial adhesins. J Bacteriol 186 : 1249 1257.
50. Schembri, M.A., Dalsgaard, D. Klemm, P. (2004b) Capsule shields the function of short bacterial adhesins. J Bacteriol 186 : 1249 1257.
51. Schembri, M.A., Blom, J., Krogfelt, K.A. Klemm, P. (2005) Capsule and fimbria interaction in Klebsiella pneumoniae. Infect Immun 73 : 4626 4633.
52. Seo, K.H. Frank, J.F. (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.
53. Sharma, M., Ryu, J.H. Beuchat, L.R. (2005) Inactivation of Escherichia coli O157:H7 in biofilm on stainless steel by treatment with an alkaline cleaner and a bacteriophage. J Appl Microbiol 99 : 449 459.
54. Sherlock, O., Schembri, M.A., Reisner, A. Klemm, P. (2004) Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. J Bacteriol 186 : 8058 8065.
55. Sherlock, O., Vejborg, R.M. Klemm, P. (2005) The TibA adhesin/invasin from enterotoxigenic Escherichia coli is self recognizing and induces bacterial aggregation and biofilm formation. Infect Immun 73 : 1954 1963.
56. Tarr, P.I., Bilge, S.S., Vary, J.C. Jr, Jelacic, S., Habeeb, R.L., Ward, T.R., et al. (2000) Iha: a novel Escherichia coli O157:H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure. Infect Immun 68 : 1400 1407.
57. Taylor, D.E., Rooker, M., Keelan, M., Ng, L.K., Martin, I., Perna, N.T., et al. (2002) Genomic variability of O islands encoding tellurite resistance in enterohemorrhagic Escherichia coli O157:H7 isolates. J Bacteriol 184 : 4690 4698.
58. Torres, A.G., Giron, J.A., Perna, N.T., Burland, V., Blattner, F.R., Avelino-Flores, F. Kaper, J.B. (2002a) Identification and characterization of lpfABCC'DE, a fimbrial operon of enterohemorrhagic Escherichia coli O157:H7. Infect Immun 70 : 5416 5427.
59. Torres, A.G., Perna, N.T., Burland, V., Ruknudin, A., Blattner, F.R. Kaper, J.B. (2002b) Characterization of Cah, a calcium-binding and heat-extractable autotransporter protein of enterohaemorrhagic Escherichia coli. Mol Microbiol 45 : 951 966.
60. Torres, A.G., Jeter, C., Langley, W. Matthysse, A.G. (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.
61. Uhlich, G.A., Keen, J.E. Elder, R.O. (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.
62. Ulett, G.C., Webb, R.I. Schembri, M.A. (2006) Antigen-43-mediated autoaggregation impairs motility in Escherichia coli. Microbiology 152 : 2101 2110.
63. Ulett, G.C., Mabbett, A.N., Fung, K.C., Webb, R.I. Schembri, M.A. (2007) The role of F9 fimbriae of uropathogenic Escherichia coli in biofilm formation. Microbiology 153 : 2321 2331.
64. Wales, A.D., Pearson, G.R., Skuse, A.M., Roe, J.M., Hayes, C.M., Cookson, A.L. Woodward, M.J. (2001) Attaching and effacing lesions caused by Escherichia coli O157:H7 in experimentally inoculated neonatal lambs. J Med Microbiol 50 : 752 758.