Sequencing and functional annotation of avian pathogenic escherichia coli serogroup O78 strains reveal the evolution of E. coli lineages pathogenic for poultry via distinct mechanisms

Infection and Immunity

Volumn 81, Issue 3, 2013, Pages 838-849

  Dziva, Francis ^a   Hauser, Heidi ^b   Connor, Thomas R ^b   van Diemen, Pauline M ^a   Prescott, Graham ^a   Langridge, Gemma C ^b   Eckert, Sabin ^b   Chaudhuri, Roy R ^c   Ewers, Christa ^d   Mellata, Melha ^e   Mukhopadhyay, Suman ^e   Curtiss III, Roy ^e   Dougan, Gordon ^b   Wieler, Lothar H ^d   Thomson, Nicholas R ^b   Pickard, Derek J ^b   Stevens, Mark P ^f  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e ARIZONA STATE UNIVERSITY   (United States)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN;

ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BIRD DISEASE; ESCHERICHIA COLI; FIMBRIA; GENE LOCUS; GENE SEQUENCE; GENETIC VARIABILITY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; POULTRY; PRIORITY JOURNAL; TRANSPOSON; TURKEY (BIRD);

ANIMALS; BIOLOGICAL EVOLUTION; DNA, BACTERIAL; ESCHERICHIA COLI; FIMBRIAE PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; LACTOFERRIN; LEUKOCYTE DISORDERS; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; POULTRY DISEASES; TURKEYS; VIRULENCE;

EID: 84874714772     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00585-12     Document Type: Article

References (88)

1. Barnes HJ, Vaiillancourt J-P, Gross WB. 2003. Colibacillosis, p 631-656. In Saif YM, Barnes HJ, Glisson JR, Fadly AM, McDougald LR (ed), Diseases of poultry, 11th ed. Iowa State University Press, Ames, IA.
2. Pires-Dos-Santos T, Bisgaard M, Christensen H. 2012. Genetic diversity and virulence profiles of Escherichia coli causing salpingitis and peritonitis in broiler breeders. Vet. Microbiol. pii:S0378-1135(12)00599-8. [Epub ahead of print.] doi:10.1016/j.vetmic.2012.11.008.
3. Olsen RH, Chadfield MS, Christensen JP, Scheutz F, Christensen H, Bisgaard M. 2011. Clonality and virulence traits of Escherichia coli associated with haemorrhagic septicaemia in turkeys. Avian Pathol. 40:587-595.
4. Johnson TJ, Kariyawasam S, Wannemuehler Y, Mangiamele P, Johnson SJ, Doetkott C, Skyberg JA, Lynne AM, Johnson JR, Nolan LK. 2007. The genome sequence of avian pathogenic Escherichia coli strain O1: K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J. Bacteriol. 189:3228-3236.
5. Bauchart P, Germon P, Brée A, Oswald E, Hacker J, Dobrindt U. 2010. Pathogenomic comparison of human extraintestinal and avian pathogenic Escherichia coli-search for factors involved in host specificity or zoonotic potential. Microb. Pathog. 49:105-115.
6. Ewers C, Antão EM, Diehl I, Philipp HC, Wieler LH. 2009. Intestine and environment of the chicken as reservoirs for extraintestinal pathogenic Escherichia coli strains with zoonotic potential. Appl. Environ. Microbiol. 75:184-192.
7. Ewers C, Li G, Wilking H, Kiessling S, Alt K, Antáo EM, Laturnus C, Diehl I, Glodde S, Homeier T, Böhnke U, Steinrück H, Philipp HC, Wieler LH. 2007. Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? Int. J. Med. Microbiol. 297:163-176.
8. Johnson TJ, Wannemuehler Y, Johnson SJ, Stell AL, Doetkott C, Johnson JR, Kim KS, Spanjaard L, Nolan LK. 2008. Comparison of extraintestinal pathogenic Escherichia coli strains from human and avian sources reveals a mixed subset representing potential zoonotic pathogens. Appl. Environ. Microbiol. 74:7043-7050.
9. Johnson TJ, Wannemuehler Y, Kariyawasam S, Johnson JR, Logue CM, Nolan LK. 2012. Prevalence of avian pathogenic Escherichia coli strain APEC O1 genomic islands among extraintestinal and commensal E. coli isolates. J. Bacteriol. 194:2846-2853.
10. Kariyawasam S, Scaccianoce JA, Nolan LK. 2007. Common and specific genomic sequences of avian and human extraintestinal pathogenic Escherichia coli as determined by genomic subtractive hybridization. BMC Microbiol. 7:81. doi:10.1186/1471-2180-7-81.
11. Mora A, López C, Dabhi G, Blanco M, Blanco JE, Alonso MP, Herrera A, Mamani R, Bonacorsi S, Moulin-Schouleur M, Blanco J. 2009. Extraintestinal pathogenic Escherichia coli O1:K1:H7/NM from human and avian origin: detection of clonal groups B2 ST95 and D ST59 with different host distribution. BMC Microbiol. 9:132. doi:10.1186/1471-2180-9-132.
12. Moriel DG, Bertoldi I, Spagnuolo A, Marchi S, Rosini R, Nesta B, Pastorello I, Corea VA, Torricelli G, Cartocci E, Savino S, Scarselli M, Dobrindt U, Hacker J, Tettelin H, Tallon LJ, Sullivan S, Wieler LH, Ewers C, Pickard D, Dougan G, Fontana MR, Rappuoli R, Pizza M, Serino L. 2010. Identification of protective and broadly conserved vaccine antigens from the genome of extraintestinal pathogenic Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 107:9072-9077.
13. Moulin-Schouleur M, Répérant M, Laurent S, Brée A, Mignon-Grasteau S, Germon P, Rasschaert D, Schouler C. 2007. Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. J. Clin. Microbiol. 45:3366-3376.
14. Tivendale KA, Logue CM, Kariyawasam S, Jordan D, Hussein A, Li G, Wannemuehler Y, Nolan LK. 2010. Avian pathogenic Escherichia coli strains are similar to neonatal meningitis E. coli strains and are able to cause meningitis in the rat model of human disease. Infect. Immun. 78: 3412-3419.
15. Li G, Laturnus C, Ewers C, Wieler LH. 2005. Identification of genes required for avian Escherichia coli septicemia by signature-tagged mutagenesis. Infect. Immun. 73:2818-2827.
16. Mellata M, Dho-Moulin M, Dozois CM, Curtiss R, III, Brown PK, Arné P, Brée A, Desautels C, Fairbrother JM. 2003. Role of virulence factors in resistance of avian pathogenic Escherichia coli to serum and in pathogenicity. Infect. Immun. 71:536-540.
17. Brown PK, Curtiss R, III. 1996. Unique chromosomal regions associated with virulence of an avian pathogenic Escherichia coli strain. Proc. Natl. Acad. Sci. U. S. A. 93:11149-11154.
18. Sabri M, Caza M, Proulx J, Lymberopoulos MH, Brée A, Moulin-Schouleur M, Curtiss R, III, Dozois CM. 2008. Contribution of the SitABCD, MntH, and FeoB metal transporters to the virulence of avian pathogenic Escherichia coli O78 strain χ7122. Infect. Immun. 76:601-611.
19. Li G, Ewers C, Laturnus C, Diehl I, Alt K, Dai J, Antão EM, Schnetz K, Wieler LH. 2008. Characterization of a yjjQ mutant of avian pathogenic Escherichia coli (APEC). Microbiology 154:1082-1093.
20. Antão EM, Ewers C, Gürlebeck D, Preisinger R, Homeier T, Li G, Wieler LH. 2009. Signature-tagged mutagenesis in a chicken infection model leads to the identification of a novel avian pathogenic Escherichia coli fimbrial adhesin. PLoS One 4:e7796. doi:10.1371/journal.pone.0007796.
21. Antão EM. 2010. Identification of avian pathogenic E. coli (APEC) genes important for the colonization of the chicken lung and characterization of the novel ExPEC adhesin I. Ph. D. thesis. Humboldt-Universität zu Berlin, Berlin, Germany. http://edoc.hu-berlin.de/dissertationen/antao-esther-maria-2010-02-08/PDF/antao.pdf.
22. Li G, Feng Y, Kariyawasam S, Tivendale KA, Wannemuehler Y, Zhou F, Logue CM, Miller CL, Nolan LK. 2010. AatA is a novel autotransporter and virulence factor of avian pathogenic Escherichia coli. Infect. Immun. 78:898-906.
23. Provence DL, Curtiss R, III. 1994. Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain. Infect. Immun. 62:1369-1380.
24. Dozois CM, Dho-Moulin M, Brée A, Fairbrother JM, Desautels C, Curtiss R, III. 2000. Relationship between the Tsh autotransporter and pathogenicity of avian Escherichia coli and localization and analysis of the Tsh genetic region. Infect. Immun. 68:4145-4154.
25. Parreira VR, Gyles CL. 2003. A novel pathogenicity island integrated adjacent to the thrW tRNA gene of avian pathogenic Escherichia coli encodes a vacuolating autotransporter toxin. Infect. Immun. 71:5087-5096.
26. Kariyawasam S, Nolan LK. 2009. Pap mutant of avian pathogenic Escherichia coli O1, an O1:K1:H7 strain, is attenuated in vivo. Avian Dis. 53: 255-260.
27. - mutant of an avian strain of Escherichia coli. Res. Microbiol. 149:473-485.
28. La Ragione RM, Sayers AR, Woodward MJ. 2000. The role of fimbriae and flagella in the colonization, invasion and persistence of Escherichia coli O78:K80 in the day-old-chick model. Epidemiol. Infect. 124:351-363.
29. Lymberopoulos MH, Houle S, Daigle F, Léveillé S, Brée A, Moulin-Schouleur M, Johnson JR, Dozois CM. 2006. Characterization of Stg fimbriae from an avian pathogenic Escherichia coli O78:K80 strain and assessment of their contribution to colonization of the chicken respiratory tract. J. Bacteriol. 188:6449-6459.
30. Ideses D, Gophna U, Paitan Y, Chaudhuri RR, Pallen MJ, Ron EZ. 2005. A degenerate type III secretion system from septicemic Escherichia coli contributes to pathogenesis. J. Bacteriol. 187:8164-8171.
31. Dozois CM, Daigle F, Curtiss R, III. 2003. Identification of pathogenspecific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc. Natl. Acad. Sci. U. S. A. 100:247-252.
32. Caza M, Lépine F, Milot S, Dozois CM. 2008. Specific roles of the iroBCDEN genes in virulence of an avian pathogenic Escherichia coli O78 strain and in production of salmochelins. Infect. Immun. 76:3539-3549.
33. Caza M, Lépine F, Dozois CM. 2011. Secretion, but not overall synthesis, of catecholate siderophores contributes to virulence of extraintestinal pathogenic Escherichia coli. Mol. Microbiol. 80:266-282.
34. Lamarche MG, Dozois CM, Daigle F, Caza M, Curtiss R, III, Dubreuil JD, Harel J. 2005. Inactivation of the pst system reduces the virulence of an avian pathogenic Escherichia coli O78 strain. Infect. Immun. 73:4138-4145.
35. Germon P, Chen YH, He L, Blanco JE, Brée A, Schouler C, Huang SH, Moulin-Schouleur M. 2005. ibeA, a virulence factor of avian pathogenic Escherichia coli. Microbiology 151:1179-1186.
36. Wang S, Shi Z, Xia Y, Li H, Kou Y, Bao Y, Dai J, Lu C. 2012. IbeB is involved in the invasion and pathogenicity of avian pathogenic Escherichia coli. Vet. Microbiol. 159:411-419.
37. Bertrand N, Houle S, LeBihan G, Poirier É, Dozois CM, Harel J. 2010. Increased Pho regulon activation correlates with decreased virulence of an avian pathogenic Escherichia coli O78 strain. Infect. Immun. 78:5324-5331.
38. Crépin S, Lamarche MG, Garneau P, Séguin J, Proulx J, Dozois CM, Harel J. 2008. Genome-wide transcriptional response of an avian pathogenic Escherichia coli (APEC) pst mutant. BMC Genomics 9:568. doi:10.1186/1471-2164-9-568.
39. Cortes MA, Gibon J, Chanteloup NK, Moulin-Schouleur M, Gilot P, Germon P. 2008. Inactivation of ibeA and ibeT results in decreased expression of type 1 fimbriae in extraintestinal pathogenic Escherichia coli strain BEN2908. Infect. Immun. 76:4129-4136.
40. Herren CD, Mitra A, Palaniyandi SK, Coleman A, Elankumaran S, Mukhopadhyay S. 2006. The BarA-UvrY two-component system regulates virulence in avian pathogenic Escherichia coli O78:K80:H9. Infect. Immun. 74:4900-4909.
41. de Pace F, Nakazato G, Pacheco A, de Paiva JB, Sperandio V, da Silveira WD. 2010. The type VI secretion system plays a role in type 1 fimbria expression and pathogenesis of an avian pathogenic Escherichia coli strain. Infect. Immun. 78:4990-4998.
42. Mellata M, Ameiss K, Mo H, Curtiss R, III. 2010. Characterization of the contribution to virulence of three large plasmids of avian pathogenic E. coli χ7122 (O78:K80:H9). Infect. Immun. 78:1528-1541.
43. Mellata M, Maddux JT, Nam T, Thomson N, Hauser H, Stevens MP, Mukhopadhyay S, Sarker S, Crabbé A, Nickerson CA, Santander J, Curtiss R, III. 2012. New insights into the bacterial fitness-associated mechanisms revealed by the characterization of large plasmids of an avian pathogenic E. coli. PLoS One 7:e29481. doi:10.1371/journal.pone.0029481.
44. Mellata M, Touchman JW, Curtiss R, III. 2009. Full sequence and comparative analysis of the plasmid pAPEC-1 of avian pathogenic E. coli χ7122 (O78:K80:H9). PLoS One 4:e4232. doi:10.1371/journal.pone.0004232.
45. Tivendale KA, Noormohammadi AH, Allen JL, Browning GF. 2009. The conserved portion of the putative virulence region contributes to virulence of avian pathogenic Escherichia coli. Microbiology 155:450-460.
46. Mellata M, Dho-Moulin M, Dozois CM, Curtiss R, III, Lehoux B, Fairbrother JM. 2003. Role of avian pathogenic Escherichia coli virulence factors in bacterial interaction with chicken heterophils and macrophages. Infect. Immun. 71:494-503.
47. Provence DL, Curtiss R, III. 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.
48. Simon R, Priefer U, Pühler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat. Biotechnol. 1:784-791.
49. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376-380.
50. Chain PS, Grafham DV, Fulton RS, Fitzgerald MG, Hostetler J, Muzny D, Ali J, Birren B, Bruce DC, Buhay C, Cole JR, Ding Y, Dugan S, Field D, Garrity GM, Gibbs R, Graves T, Han CS, Harrison SH, Highlander S, Hugenholtz P, Khouri HM, Kodira CD, Kolker E, Kyrpides NC, Lang D, Lapidus A, Malfatti SA, Markowitz V, Metha T, Nelson KE, Parkhill J, Pitluck S, Qin X, Read TD, Schmutz J, Sozhamannan S, Sterk P, Strausberg RL, Sutton G, Thomson NR, Tiedje JM, Weinstock G, Wollam A, Genomic Standards Consortium Human Microbiome Project Jumpstart Consortium, Detter JC. 2009. Genome project standards in a new era of sequencing. Science 326:236-237.
51. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945.
52. Berriman M, Rutherford K. 2003. Viewing and annotating sequence data with Artemis. Brief. Bioinform. 4:124-132.
53. Riley M, Abe T, Arnaud MB, Berlyn MK, Blattner FR, Chaudhuri RR, Glasner JD, Horiuchi T, Keseler IM, Kosuge T, Mori H, Perna NT, Plunkett G, III, Rudd KE, Serres MH, Thomas GH, Thomson NR, Wishart D, Wanner BL. 2006. Escherichia coli K-12: a cooperatively developed annotation snapshot-2005. Nucleic Acids Res. 34:1-9.
54. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. doi:10.1186/1471-2105-11-119.
55. Li L, Stoeckert CJ, Jr, Roos DS. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-2189. 56. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. 2005. ACT: the Artemis Comparison Tool. Bioinformatics 21:3422-3423.
56. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. 2005. ACT: the Artemis Comparison Tool. Bioinformatics 21:3422-3423.
57. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18:821-829.
58. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
59. Liu K, Linder CR, Warnow T. 2011. RAxML and FastTree: comparing two methods for large-scale maximum likelihood phylogeny estimation. PLoS One 6:e27731. doi:10.1371/journal.pone.0027731.
60. Dziva F, van Diemen PM, Stevens MP, Smith AJ, Wallis TS. 2004. Identification of Escherichia coli O157:H7 genes influencing colonization of the bovine gastrointestinal tract using signature-tagged mutagenesis. Microbiology 150:3631-3645.
61. Barrow PA. 1983. A note on a method to aid sampling populations for characteristics. J. Appl. Bacteriol. 54:311-312.
62. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
63. Ren CP, Chaudhuri RR, Fivian A, Bailey CM, Antonio M, Barnes WM, Pallen MJ. 2004. The ETT2 gene cluster, encoding a second type III secretion system from Escherichia coli, is present in the majority of strains but has undergone widespread mutational attrition. J. Bacteriol. 186:3547-3560.
64. Peleg A, Shifrin Y, Ilan O, Nadler-Yona C, Nov S, Koby S, Baruch K, Altuvia S, Elgrably-Weiss M, Abe CM, Knutton S, Saper MA, Rosenshine I. 2005. Identification of an Escherichia coli operon required for formation of the O-antigen capsule. J. Bacteriol. 187:5259-5266.
65. Korea CG, Badouraly R, Prevost MC, Ghigo JM, Beloin C. 2010. Escherichia coli K-12 possesses multiple cryptic but functional chaperoneusher fimbriae with distinct surface specificities. Environ. Microbiol. 12: 1957-1977.
66. Brzuszkiewicz E, Brüggemann H, Liesegang H, Emmerth M, Olschläger T, Nagy G, Albermann K, Wagner C, Buchrieser C, Emody L, Gottschalk G, Hacker J, Dobrindt U. 2006. How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc. Natl. Acad. Sci. U. S. A. 103:12879-12884.
67. Lynne AM, Skyberg JA, Logue CM, Nolan LK. 2007. Detection of Iss and Bor on the surface of Escherichia coli. J. Appl. Microbiol. 102:660-666. 68. Binns MM, Davies DL, Hardy KG. 1979. Cloned fragments of the plasmid ColV,I-K94 specifying virulence and serum resistance. Nature 279: 778-781.
68. Binns MM, Davies DL, Hardy KG. 1979. Cloned fragments of the plasmid ColV,I-K94 specifying virulence and serum resistance. Nature 279: 778-781.
69. Barondess JJ, Beckwith J. 1990. A bacterial virulence determinant encoded by lysogenic coliphage lambda. Nature 346:871-874.
70. Skyberg JA, Johnson TJ, Nolan LK. 2008. Mutational and transcriptional analyses of an avian pathogenic Escherichia coli ColV plasmid. BMC Microbiol. 8:24. doi:10.1186/1471-2180-8-24.
71. Lynne AM, Skyberg JA, Logue CM, Doetkott C, Foley SL, Nolan LK. 2007. Characterization of a series of transconjugant mutants of an avian pathogenic Escherichia coli isolate for resistance to serum complement. Avian Dis. 51:771-776.
72. Li G, Tivendale KA, Liu P, Feng Y, Wannemuehler Y, Cai W, Mangiamele P, Johnson TJ, Constantinidou C, Penn CW, Nolan LK, Payne SM. 2011. Transcriptome analysis of avian pathogenic Escherichia coli O1 in chicken serum reveals adaptive responses to systemic infection. Infect. Immun. 79:1951-1960.
73. Badger JL, Wass CA, Kim KS. 2000. Identification of Escherichia coli K1 genes contributing to human brain microvascular endothelial cell invasion by differential fluorescence induction. Mol. Microbiol. 36:174-182.
74. Badger JL, Wass CA, Weissman SJ, Kim KS. 2000. Application of signature-tagged mutagenesis for identification of Escherichia coli K1 genes that contribute to invasion of human brain microvascular endothelial cells. Infect. Immun. 68:5056-5061.
75. Hill VT, Townsend SM, Arias RS, Jenabi JM, Gomez-Gonzalez I, Shimada H, Badger JL. 2004. TraJ-dependent Escherichia coli K1 interactions with professional phagocytes are important for early systemic dissemination of infection in the neonatal rat. Infect. Immun. 72:478-488.
76. Martindale J, Stroud D, Moxon ER, Tang CM. 2000. Genetic analysis of Escherichia coli K1 gastrointestinal colonization. Mol. Microbiol. 37:1293-1305.
77. Gonzalez MD, Lichtensteiger CA, Vimr ER. 2001. Adaptation of signature-tagged mutagenesis to Escherichia coli K1 and the infant-rat model of invasive disease. FEMS Microbiol. Lett. 198:125-128.
78. Bahrani-Mougeot FK, Buckles EL, Lockatell CV, Hebel JR, Johnson DE, Tang CM, Donnenberg MS. 2002. Type 1 fimbriae and extracellular polysaccharides are preeminent uropathogenic Escherichia coli virulence determinants in the murine urinary tract. Mol. Microbiol. 45:1079-1093.
79. Tuntufye HN, Lebeer S, Gwakisa PS, Goddeeris BM. 2012. Identification of avian pathogenic Escherichia coli genes that are induced in vivo during infection in chickens. Appl. Environ. Microbiol. 78:3343-3351.
80. Shifrin Y, Peleg A, Ilan O, Nadler C, Kobi S, Baruch K, Yerushalmi G, Berdichevsky T, Altuvia S, Elgrably-Weiss M, Abe C, Knutton S, Sasakawa C, Ritchie JM, Waldor MK, Rosenshine I. 2008. Transient shielding of intimin and the type III secretion system of enterohemorrhagic and enteropathogenic Escherichia coli by a group 4 capsule. J. Bacteriol. 190:5063-5074.
81. Girón JA, Torres AG, Freer E, Kaper JB. 2002. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol. Microbiol. 44:361-379.
82. Erdem AL, Avelino F, Xicohtencatl-Cortes J, Girón JA. 2007. Host protein binding and adhesive properties of H6 and H7 flagella of attaching and effacing Escherichia coli. J. Bacteriol. 189:7426-7435.
83. Mahajan A, Currie CG, Mackie S, Tree J, McAteer S, McKendrick I, McNeilly TN, Roe A, La Ragione RM, Woodward MJ, Gally DL, Smith DG. 2009. An investigation of the expression and adhesin function of H7 flagella in the interaction of Escherichia coli O157:H7 with bovine intestinal epithelium. Cell. Microbiol. 11:121-137.
84. Masuda N, Church GM. 2002. Escherichia coli gene expression responsive to levels of the response regulator EvgA. J. Bacteriol. 184:6225-6234. 85. Nishino K, Inazumi Y, Yamaguchi A. 2003. Global analysis of gene regulation by EvgA of the two-component regulatory system of Escherichia coli. J. Bacteriol. 185:2667-2672.
85. Nishino K, Inazumi Y, Yamaguchi A. 2003. Global analysis of gene regulation by EvgA of the two-component regulatory system of Escherichia coli. J. Bacteriol. 185:2667-2672.
86. Low AS, Holden N, Rosser T, Roe AJ, Constantinidou C, Hobman JL, Smith DG, Low JC, Gally DL. 2006. Analysis of fimbrial gene clusters and their expression in enterohaemorrhagic Escherichia coli O157:H7. Environ. Microbiol. 8:1033-1047.
87. Spurbeck RR, Stapleton AE, Johnson JR, Walk ST, Hooton TM, Mobley HL. 2011. Fimbrial profiles predict virulence of uropathogenic Escherichia coli strains: contribution of ygi and yad fimbriae. Infect. Immun. 79:4753-4763.
88. Torres AG. 2009. The cad locus of Enterobacteriaceae: more than just lysine decarboxylation. Anaerobe 15:1-6.