1887

Abstract

Autotransporter (AT) proteins are found in all pathotypes and are often associated with virulence. In this study we took advantage of the large number of available genome sequences to perform an in-depth bioinformatic analysis of AT-encoding genes. Twenty-eight genome sequences were probed using an iterative approach, which revealed a total of 215 AT-encoding sequences that represented three major groups of distinct domain architecture: (i) serine protease AT proteins, (ii) trimeric AT adhesins and (iii) AIDA-I-type AT proteins. A number of subgroups were identified within each broad category, and most subgroups contained at least one characterized AT protein; however, seven subgroups contained no previously described proteins. The AIDA-I-type AT proteins represented the largest and most diverse group, with up to 16 subgroups identified from sequence-based comparisons. Nine of the AIDA-I-type AT protein subgroups contained at least one protein that possessed functional properties associated with aggregation and/or biofilm formation, suggesting a high degree of redundancy for this phenotype. The Ag43, YfaL/EhaC, EhaB/UpaC and UpaG subgroups were found in nearly all strains. Among the remaining subgroups, there was a tendency for AT proteins to be associated with individual pathotypes, suggesting that they contribute to tissue tropism or symptoms specific to different disease outcomes.

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2010-08-01
2020-01-22
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References

  1. Allsopp, L. P., Totsika, M., Tree, J. J., Ulett, G. C., Mabbett, A. N., Wells, T. J., Kobe, B., Beatson, S. B. & Schembri, M. A. ( 2010; ). UpaH is a newly identified autotransporter protein that contributes to biofilm formation and bladder colonization by uropathogenic Escherichia coli CFT073. Infect Immun 78, 1659–1669.[CrossRef]
    [Google Scholar]
  2. 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.[CrossRef]
    [Google Scholar]
  3. Benz, I. & Schmidt, M. A. ( 1989; ). Cloning and expression of an adhesin (Aida-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect Immun 57, 1506–1511.
    [Google Scholar]
  4. Benz, I. & Schmidt, M. A. ( 1992; ). Isolation and serologic characterization of Aida-I, the adhesin mediating the diffuse adherence phenotype of the diarrhea-associated Escherichia coli strain-2787 (O126 : H27). Infect Immun 60, 13–18.
    [Google Scholar]
  5. Blattner, F. R., Plunkett, G., III, Bloch, C. A., Perna, N. T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J. D., Rode, C. K. & other authors ( 1997; ). The complete genome sequence of Escherichia coli K-12. Science 277, 1453–1462.[CrossRef]
    [Google Scholar]
  6. Brunder, W., Schmidt, H. & Karch, H. ( 1997; ). EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157 : H7 cleaves human coagulation factor V. Mol Microbiol 24, 767–778.[CrossRef]
    [Google Scholar]
  7. Chen, S. L., Hung, C.-S., Xu, J., Reigstad, C. S., Magrini, V., Sabo, A., Blasiar, D., Bieri, T., Meyer, R. R. & other authors ( 2006; ). Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad Sci U S A 103, 5977–5982.[CrossRef]
    [Google Scholar]
  8. Cotter, S. E., Surana, N. K. & St Geme, J. W. ( 2005; ). Trimeric autotransporters: a distinct subfamily of autotransporter proteins. Trends Microbiol 13, 199–205.[CrossRef]
    [Google Scholar]
  9. Desvaux, M., Parham, N. J. & Henderson, I. R. ( 2004; ). The autotransporter secretion system. Res Microbiol 155, 53–60.[CrossRef]
    [Google Scholar]
  10. Djafari, S., Ebel, F., Deibel, C., Kramer, S., Hudel, M. & Chakraborty, T. ( 1997; ). Characterization of an exported protease from Shiga toxin-producing Escherichia coli. Mol Microbiol 25, 771–784.[CrossRef]
    [Google Scholar]
  11. Eichler, E. E. ( 2001; ). Segmental duplications: what's missing, misassigned, and misassembled – and should we care? Genome Res 11, 653–656.[CrossRef]
    [Google Scholar]
  12. Elsinghorst, E. A. & Weitz, J. A. ( 1994; ). Epithelial-cell invasion and adherence directed by the enterotoxigenic Escherichia coli tib locus is associated with a 104-kilodalton outer-membrane protein. Infect Immun 62, 3463–3471.
    [Google Scholar]
  13. Emsley, P., McDermott, G., Charles, I. G., Fairweather, N. F. & Isaacs, N. W. ( 1994; ). Crystallographic characterization of pertactin, a membrane-associated protein from Bordetella pertussis. J Mol Biol 235, 772–773.[CrossRef]
    [Google Scholar]
  14. Emsley, P., Charles, I. G., Fairweather, N. F. & Isaacs, N. W. ( 1996; ). Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381, 90–92.[CrossRef]
    [Google Scholar]
  15. Eslava, C., Navarro-Garcia, F., Czeczulin, J. R., Henderson, I. R., Cravioto, A. & Nataro, J. P. ( 1998; ). Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect Immun 66, 3155–3163.
    [Google Scholar]
  16. Fernandez, R. C. & Weiss, A. A. ( 1994; ). Cloning and sequencing of a Bordetella pertussis serum resistance locus. Infect Immun 62, 4727–4738.
    [Google Scholar]
  17. Guyer, D. M., Henderson, I. R., Nataro, J. P. & Mobley, H. L. T. ( 2000; ). Identification of Sat, an autotransporter toxin produced by uropathogenic Escherichia coli. Mol Microbiol 38, 53–66.[CrossRef]
    [Google Scholar]
  18. Guyer, D. M., Radulovic, S., Jones, F. E. & Mobley, H. L. T. ( 2002; ). Sat, the secreted autotransporter toxin of uropathogenic Escherichia coli, is a vacuolating cytotoxin for bladder and kidney epithelial cells. Infect Immun 70, 4539–4546.[CrossRef]
    [Google Scholar]
  19. Hasman, H., Chakraborty, T. & Klemm, P. ( 1999; ). Antigen-43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J Bacteriol 181, 4834–4841.
    [Google Scholar]
  20. Henderson, I. R. & Nataro, J. P. ( 2001; ). Virulence functions of autotransporter proteins. Infect Immun 69, 1231–1243.[CrossRef]
    [Google Scholar]
  21. Henderson, I. R. & Owen, P. ( 1999; ). The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin A1 protease class of exported protein and is regulated by a novel mechanism involving Dam and OxyR. J Bacteriol 181, 2132–2141.
    [Google Scholar]
  22. 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.[CrossRef]
    [Google Scholar]
  23. 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.[CrossRef]
    [Google Scholar]
  24. Hochhut, B., Wilde, C., Balling, G., Middendorf, B., Dobrindt, U., Brzuszkiewicz, E., Gottschalk, G., Carniel, E. & Hacker, J. ( 2006; ). Role of pathogenicity island-associated integrases in the genome plasticity of uropathogenic Escherichia coli strain 536. Mol Microbiol 61, 584–595.[CrossRef]
    [Google Scholar]
  25. Hoiczyk, E., Roggenkamp, A., Reichenbecher, M., Lupas, A. & Heesemann, J. ( 2000; ). Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 19, 5989–5999.[CrossRef]
    [Google Scholar]
  26. Ieva, R. & Bernstein, H. D. ( 2009; ). Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc Natl Acad Sci U S A 106, 19120–19125.[CrossRef]
    [Google Scholar]
  27. Iguchi, A., Thomson, N. R., Ogura, Y., Saunders, D., Ooka, T., Henderson, I. R., Harris, D., Asadulghani, M., Kurokawa, K. & other authors ( 2009; ). Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127 : H6 strain E2348/69. J Bacteriol 191, 347–354.[CrossRef]
    [Google Scholar]
  28. Johnson, T. J., Wannemeuhler, Y. M., Scaccianoce, J. A., Johnson, S. J. & Nolan, L. K. ( 2006; ). Complete DNA sequence, comparative genomics, and prevalence of an IncHI2 plasmid occurring among extraintestinal pathogenic Escherichia coli isolates. Antimicrob Agents Chemother 50, 3929–3933.[CrossRef]
    [Google Scholar]
  29. Jose, J., Jahnig, F. & Meyer, T. F. ( 1995; ). Common structural features of Iga1 protease-like outer-membrane protein autotransporters. Mol Microbiol 18, 378–380.[CrossRef]
    [Google Scholar]
  30. Kajava, A. V., Cheng, N., Cleaver, R., Kessel, M., Simon, M. N., Willery, E., Jacob-Dubuisson, F., Locht, C. & Steven, A. C. ( 2001; ). Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42, 279–292.[CrossRef]
    [Google Scholar]
  31. Kjaergaard, K., Schembri, M. A., Ramos, C., Molin, S. & Klemm, P. ( 2000; ). Antigen 43 facilitates formation of multispecies biofilms. Environ Microbiol 2, 695–702.[CrossRef]
    [Google Scholar]
  32. 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.
    [Google Scholar]
  33. Klemm, P., Vejborg, R. M. & Sherlock, O. ( 2006; ). Self-associating autotransporters, SAATs: functional and structural similarities. Int J Med Microbiol 296, 187–195.[CrossRef]
    [Google Scholar]
  34. Leyton, D. L., Sloan, J., Hill, R. E., Doughty, S. & Hartland, E. L. ( 2003; ). Transfer region of pO113 from enterohemorrhagic Escherichia coli: similarity with R64 and identification of a novel plasmid-encoded autotransporter, EpeA. Infect Immun 71, 6307–6319.[CrossRef]
    [Google Scholar]
  35. Leyton, D. L., Adams, L. M., Kelly, M., Sloan, J., Tauschek, M., Robins-Browne, R. M. & Hartland, E. L. ( 2007; ). Contribution of a novel gene, rpeA, encoding a putative autotransporter adhesin to intestinal colonization by rabbit-specific enteropathogenic Escherichia coli. Infect Immun 75, 4664–4669.[CrossRef]
    [Google Scholar]
  36. Li, G., Feng, Y., Kariyawasam, S., Tivendale, K. A., Wannemuehler, Y., Zhou, F., Logue, C. M., Miller, C. L. & Nolan, L. K. ( 2010; ). AatA is a novel autotransporter and virulence factor of avian pathogenic Escherichia coli. Infect Immun 78, 898–906.[CrossRef]
    [Google Scholar]
  37. Lindenthal, C. & Elsinghorst, E. A. ( 2001; ). Enterotoxigenic Escherichia coli TibA glycoprotein adheres to human intestine epithelial cells. Infect Immun 69, 52–57.[CrossRef]
    [Google Scholar]
  38. Linke, D., Riess, T., Autenrieth, I. B., Lupas, A. & Kempf, V. A. J. ( 2006; ). Trimeric autotransporter adhesins: variable structure, common function. Trends Microbiol 14, 264–270.[CrossRef]
    [Google Scholar]
  39. Loomis, W. F. & Fuller, D. L. ( 1990; ). A pair of tandemly repeated genes code for gp24, a putative adhesion protein of Dictyostelium discoideum. Proc Natl Acad Sci U S A 87, 886–890.[CrossRef]
    [Google Scholar]
  40. Loveless, B. J. & Saier, M. H. ( 1997; ). A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol Membr Biol 14, 113–123.[CrossRef]
    [Google Scholar]
  41. Lu, Y., Iyoda, S., Satou, H., Satou, H., Itoh, K., Saitoh, T. & Watanabe, H. ( 2006; ). A new immunoglobulin-binding protein, EibG, is responsible for the chain-like adhesion phenotype of locus of enterocyte effacement-negative, Shiga toxin-producing Escherichia coli. Infect Immun 74, 5747–5755.[CrossRef]
    [Google Scholar]
  42. Luthje, P. & Brauner, A. ( 2010; ). Putative link between the virulence-associated fluA gene and fluoroquinolone resistance in uropathogenic Escherichia coli. J Clin Microbiol 48, 675–676.[CrossRef]
    [Google Scholar]
  43. Makino, K., Yokoyama, K., Kubota, Y., Yutsudo, C. H., Kimura, S., Kurokawa, K., Ishii, K., Hattori, M., Tatsuno, I. & other authors ( 1999; ). Complete nucleotide sequence of the prophage VT2-Sakai carrying the verotoxin 2 genes of the enterohemorrhagic Escherichia coli O157 : H7 derived from the Sakai outbreak. Genes Genet Syst 74, 227–239.[CrossRef]
    [Google Scholar]
  44. Mellies, J. L., Navarro-Garcia, F., Okeke, I., Frederickson, J., Nataro, J. P. & Kaper, J. B. ( 2001; ). espC pathogenicity island of enteropathogenic Escherichia coli encodes an enterotoxin. Infect Immun 69, 315–324.[CrossRef]
    [Google Scholar]
  45. Naylor, S. W., Low, J. C., Besser, T. E., Mahajan, A., Gunn, G. J., Pearce, M. C., McKendrick, I. J., Smith, D. G. & Gally, D. L. ( 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.[CrossRef]
    [Google Scholar]
  46. Nummelin, H., Merckel, M. C., Leo, J. C., Lankinen, H., Skurnik, M. & Goldman, A. ( 2004; ). The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel β-roll. EMBO J 23, 701–711.[CrossRef]
    [Google Scholar]
  47. Otto, B. R., van Dooren, S. J. M., Nuijens, J. H., Luirink, J. & Oudega, B. ( 1998; ). Characterization of a hemoglobin protease secreted by the pathogenic Escherichia coli strain EB1. J Exp Med 188, 1091–1103.[CrossRef]
    [Google Scholar]
  48. Parham, N. J., Srinivasan, U., Desvaux, M., Foxman, B., Marrs, C. F. & Henderson, I. R. ( 2004; ). PicU, a second serine protease autotransporter of uropathogenic Escherichia coli. FEMS Microbiol Lett 230, 73–83.[CrossRef]
    [Google Scholar]
  49. Patel, S. K., Dotson, J., Allen, K. P. & Fleckenstein, J. M. ( 2004; ). Identification and molecular characterization of EatA, an autotransporter protein of enterotoxigenic Escherichia coli. Infect Immun 72, 1786–1794.[CrossRef]
    [Google Scholar]
  50. Paton, A. W., Srimanote, P., Woodrow, M. C. & Paton, J. C. ( 2001; ). Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect Immun 69, 6999–7009.[CrossRef]
    [Google Scholar]
  51. Perna, N. T., Plunkett, G., III, Burland, V., Mau, B., Glasner, J. D., Rose, D. J., Mayhew, G. F., Evans, P. S., Gregor, J. & other authors ( 2001; ). Genome sequence of enterohaemorrhagic Escherichia coli O157 : H7. Nature 409, 529–533.[CrossRef]
    [Google Scholar]
  52. Provence, D. L. & Curtiss, R. ( 1994; ). Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain. Infect Immun 62, 1369–1380.
    [Google Scholar]
  53. Relman, D. A., Domenighini, M., Tuomanen, E., Rappuoli, R. & Falkow, S. ( 1989; ). Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc Natl Acad Sci U S A 86, 2637–2641.[CrossRef]
    [Google Scholar]
  54. Reyrat, J. M., Pelicic, V., Papini, E., Montecucco, C., Rappuoli, R. & Telford, J. L. ( 1999; ). Towards deciphering the Helicobacter pylori cytotoxin. Mol Microbiol 34, 197–204.[CrossRef]
    [Google Scholar]
  55. Riess, T., Andersson, S. G., Lupas, A., Schaller, M., Schäfer, A., Kyme, P., Martin, J., Wälzlein, J. H., Ehehalt, U. & other authors ( 2004; ). Bartonella adhesin a mediates a proangiogenic host cell response. Exp Med 200, 1267–1278.[CrossRef]
    [Google Scholar]
  56. Roggenkamp, A., Ackermann, N., Jacobi, C. A., Truelzsch, K., Hoffmann, H. & Heesemann, H. ( 2003; ). Molecular analysis of transport and oligomerization of the Yersinia enterocolitica adhesin YadA. J Bacteriol 185, 3735–3744.[CrossRef]
    [Google Scholar]
  57. 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.[CrossRef]
    [Google Scholar]
  58. Ruiz-Perez, F., Henderson, I. R., Leyton, D. L., Rossiter, A. E., Zhang, Y. H. & Nataro, J. P. ( 2009; ). Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J Bacteriol 191, 6571–6583.[CrossRef]
    [Google Scholar]
  59. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  60. Salzberg, S. L. & Yorke, J. A. ( 2005; ). Beware of mis-assembled genomes. Bioinformatics 21, 4320–4321.[CrossRef]
    [Google Scholar]
  61. Sandt, C. H. & Hill, C. W. ( 2000; ). Four different genes responsible for nonimmune immunoglobulin-binding activities within a single strain of Escherichia coli. Infect Immun 68, 2205–2214.[CrossRef]
    [Google Scholar]
  62. Sandt, C. H. & Hill, C. W. ( 2001; ). Nonimmune binding of human immunoglobulin A (IgA) and IgG Fc by distinct sequence segments of the EibF cell surface protein of Escherichia coli. Infect Immun 69, 7293–7303.[CrossRef]
    [Google Scholar]
  63. Sandt, C. H., Wang, Y. D., Wilson, R. A. & Hill, C. W. ( 1997; ). Escherichia coli strains with nonimmune immunoglobulin-binding activity. Infect Immun 65, 4572–4579.
    [Google Scholar]
  64. Sauri, A., Soprova, Z., Wickstrom, D., de Gier, J.-W., Van der Schors, R. C., Smit, A. B., Jong, W. S. P. & Luirink, J. ( 2009; ). The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease. Microbiology 155, 3982–3991.[CrossRef]
    [Google Scholar]
  65. 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.[CrossRef]
    [Google Scholar]
  66. 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.[CrossRef]
    [Google Scholar]
  67. Stein, M., Kenny, B., Stein, M. A. & Finlay, B. B. ( 1996; ). Characterization of EspC, a 110-kilodalton protein secreted by enteropathogenic Escherichia coli which is homologous to members of the immunoglobulin A protease-like family of secreted proteins. J Bacteriol 178, 6546–6554.
    [Google Scholar]
  68. Surana, N. K., Cutter, D., Barenkamp, S. J. & St Geme, J. W. ( 2004; ). The Haemophilus influenzae Hia autotransporter contains an unusually short trimeric translocator domain. J Biol Chem 279, 14679–14685.[CrossRef]
    [Google Scholar]
  69. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. ( 1997; ). The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef]
    [Google Scholar]
  70. Torres, A. G., Perna, N. T., Burland, V., Ruknudin, A., Blattner, F. R. & Kaper, J. B. ( 2002; ). Characterization of Cah, a calcium-binding and heat-extractable autotransporter protein of enterohaemorrhagic Escherichia coli. Mol Microbiol 45, 951–966.[CrossRef]
    [Google Scholar]
  71. Touchon, M., Hoede, C., Tenaillon, O., Barbe, V., Baeriswyl, S., Bidet, P., Bingen, E., Bonacorsi, S., Bouchier, C. & other authors ( 2009; ). Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5, e1000344 [CrossRef]
    [Google Scholar]
  72. Ulett, G. C., Webb, R. I. & Schembri, M. A. ( 2006; ). Antigen-43-mediated autoaggregation impairs motility in Escherichia coli. Microbiology 152, 2101–2110.[CrossRef]
    [Google Scholar]
  73. 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.[CrossRef]
    [Google Scholar]
  74. Valle, J., Mabbett, A. N., Ulett, G. C., Toledo-Arana, A., Wecker, K., Totsika, M., Schembri, M. A., Ghigo, J.-M. & Beloin, C. ( 2008; ). UpaG, a new member of the trimeric autotransporter family of adhesins in uropathogenic Escherichia coli. J Bacteriol 190, 4147–4161.
  75. Wagner, J. K., Heindl, J. E., Gray, A. N., Jain, S. & Goldberg, M. B. ( 2009; ). Contribution of the periplasmic chaperone Skp to efficient presentation of the autotransporter IcsA on the surface of Shigella flexneri. J Bacteriol 191, 815–821.[CrossRef]
    [Google Scholar]
  76. Welch, R. A., Burland, V., Plunkett, G., Redford, P., Roesch, P., Rasko, D., Buckles, E. L., Liou, S. R., Boutin, A. & other authors ( 2002; ). Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 99, 17020–17024.[CrossRef]
    [Google Scholar]
  77. Wells, T. J., Sherlock, O., Rivas, L., Mahajan, A., Beatson, S. A., Torpdahl, M., Webb, R. I., Allsopp, L. P., Gobius, K. S. & other authors ( 2008; ). EhaA is a novel autotransporter protein of enterohemorrhagic Escherichia coli O157 : H7 that contributes to adhesion and biofilm formation. Environ Microbiol 10, 589–604.[CrossRef]
    [Google Scholar]
  78. Wells, T. J., McNeilly, T. N., Totsika, M., Mahajan, A., Gally, D. L. & Schembri, M. A. ( 2009; ). The Escherichia coli O157 : H7 EhaB autotransporter protein binds to laminin and collagen I and induces a serum IgA response in O157 : H7 challenged cattle. Environ Microbiol 11, 1803–1814.[CrossRef]
    [Google Scholar]
  79. Yen, M. R., Peabody, C. R., Partovi, S. M., Zhai, Y. F., Tseng, Y. H. & Saier, M. H. ( 2002; ). Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim Biophys Acta 1562, 6–31.[CrossRef]
    [Google Scholar]
  80. Yeo, H. J., Cotter, S. E., Laarmann, S., Juehne, T., St Geme, J. W. & Waksman, G. ( 2004; ). Structural basis for host recognition by the Haemophilus influenzae Hia autotransporter. EMBO J 23, 1245–1256.[CrossRef]
    [Google Scholar]
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