Genome sequence of adherent-invasive Escherichia coli and comparative genomic analysis with other E. coli pathotypes

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Nash, John H E ^a   Villegas, Andre ^a   Kropinski, Andrew M ^a   Aguilar Valenzuela, Renan ^b   Konczy, Paulina ^a   Mascarenhas, Mariola ^a   Ziebell, Kim ^a   Torres, Alfredo G ^b   Karmali, Mohamed A ^a   Coombes, Brian K ^c  

^a PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^b University of Texas Medical Branch School of Medicine   (United States)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; CROHN DISEASE; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; FEMALE; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC LINKAGE; ILEUM; MENINGITIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; URINARY TRACT INFECTION; BACTERIAL GENE; BACTERIUM ADHERENCE; CLASSIFICATION; COMPARATIVE STUDY; DNA SEQUENCE; GENETICS; GENOMIC ISLAND; GENOMICS; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; MUTATION; PATHOGENICITY; PLASMID; TRANSPORT AT THE CELLULAR LEVEL; VIRULENCE;

ESCHERICHIA COLI;

IRON; VIRULENCE FACTOR;

BACTERIAL ADHESION; BASE SEQUENCE; BIOLOGICAL TRANSPORT; ESCHERICHIA COLI; GENES, BACTERIAL; GENOME, BACTERIAL; GENOMIC ISLANDS; GENOMICS; IRON; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PLASMIDS; SEQUENCE ANALYSIS, DNA; VIRULENCE; VIRULENCE FACTORS;

EID: 78649335559     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-667     Document Type: Article

References (79)

1. Sartor RB. Current concepts of the etiology and pathogenesis of ulcerative colitis and Crohn's disease. Gastroenterol Clin North Am 1995, 24:475-507.
2. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007, 448:427-434. 10.1038/nature06005, 17653185.
3. Campieri M, Gionchetti P. Bacteria as the cause of ulcerative colitis. Gut 2001, 48:132-135. 10.1136/gut.48.1.132, 1728175, 11115835.
4. Strober W, Fuss IJ, Blumberg RS. The immunology of mucosal models of inflammation. Annu Rev Immunol 2002, 20:495-549. 10.1146/annurev.immunol.20.100301.064816, 11861611.
5. Giaffer M, Holdsworth C, Duerden B. Virulence properties of Escherichia coli strains isolated from patients with inflammatory bowel disease. Gut 1992, 33:646-650. 10.1136/gut.33.5.646, 1379295, 1612481.
6. Liu SL, Sanderson KE. I-CeuI reveals conservation of the genome of independent strains of Salmonella typhimurium. J Bacteriol 1995, 177:3355-3357. 177035, 7768842.
7. Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser AL, Barnich N, Bringer MA, Swidsinski A, Beaugerie L, Colombel JF. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 2004, 127:412-421. 10.1053/j.gastro.2004.04.061, 15300573.
8. Martin H, Campbell B, Hart C, Mpofu C, Nayar M. Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology 2004, 127:80-93. 10.1053/j.gastro.2004.03.054, 15236175.
9. Darfeuille-Michaud A. Adherent-invasive Escherichia coli: a putative new E. coli pathotype associated with Crohn's disease. Int J Med Microbiol 2002, 292:185-193. 10.1078/1438-4221-00201, 12398209.
10. Boudeau J, Glasser A, Masseret E, Joly B. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect Immun 1999, 67:4499-4509. 96770, 10456892.
11. Schultsz C, van den Berg F, ten Kate F, Tytgat G. The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls. Gastroenterology 1999, 117:1089-1097. 10.1016/S0016-5085(99)70393-8, 10535871.
12. Darfeuille-Michaud A, Neut C, Barnich N, Lederman E, Di Martino P, Desreumaux P, Gambiez L, Joly B, Cortot A, Colombel JF. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 1998, 115:1405-1413. 10.1016/S0016-5085(98)70019-8, 9834268.
13. Rolhion N, Darfeuille-Michaud A. Adherent-invasive Escherichia coli in inflammatory bowel disease. Inflamm Bowel Dis 2007, 13:1277-1283. 10.1002/ibd.20176, 17476674.
14. Carvalho FA, Barnich N, Sivignon A, Darcha C, Chan CH, Stanners CP, Darfeuille-Michaud A. Crohn's disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med 2009, 206:2179-2189. 10.1084/jem.20090741, 2757893, 19737864.
15. Barnich N, Darfeuille-Michaud A. Adherent-invasive Escherichia coli and Crohn's disease. Curr Opin Gastroenterol 2007, 23:16-20. 10.1097/MOG.0b013e3280105a38, 17133079.
16. Eaves-Pyles T, Allen CA, Taormina J, Swidsinski A, Tutt CB, Jezek GE, Islas-Islas M, Torres AG. Escherichia coli isolated from a Crohn's disease patient adheres, invades, and induces inflammatory responses in polarized intestinal epithelial cells. Int J Med Microbiol 2008, 298:397-409. 10.1016/j.ijmm.2007.05.011, 17900983.
17. Martinez-Medina M, Mora A, Blanco M, Lopez C, Alonso MP, Bonacorsi S, Nicolas-Chanoine MH, Darfeuille-Michaud A, Garcia-Gil J, Blanco J. Similarity and divergence among adherent-invasive Escherichia coli and extraintestinal pathogenic E. coli strains. J Clin Microbiol 2009, 47:3968-3979. 10.1128/JCM.01484-09, 2786640, 19828750.
18. Konczy P, Ziebell K, Mascarenhas M, Choi A, Michaud C, Kropinski AM, Whittam TS, Wickham M, Finlay B, Karmali MA. Genomic O island 122, locus for enterocyte effacement, and the evolution of virulent verocytotoxin-producing Escherichia coli. J Bacteriol 2008, 190:5832-5840. 10.1128/JB.00480-08, 2519529, 18586943.
19. Rasko DA, Rosovitz MJ, Myers GS, Mongodin EF, Fricke WF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R, et al. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 2008, 190:6881-6893. 10.1128/JB.00619-08, 2566221, 18676672.
20. Gross WB. Diseases due to Escherichia coli in poultry. Escherichia coli in domestic animals and humans 1994, 237-259. C.L. G. Wallingford, UK: CAB International.
21. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nature Reviews Microbiology 2004, 2:123-140. 10.1038/nrmicro818, 15040260.
22. Russo TA, Johnson JR. Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis 2000, 181:1753-1754. 10.1086/315418, 10823778.
23. Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2010, 8:26-38.
24. Antão EM, Wieler LH, Ewers C. Adhesive threads of extraintestinal pathogenic Escherichia coli. Gut Pathog 2009, 1:22. 10.1186/1757-4749-1-22, 2797515, 20003270.
25. Kim KS. Pathogenesis of bacterial meningitis: From bacteraemia to neuronal injury. Nature Reviews Neuroscience 2003, 4:376-385. 10.1038/nrn1103, 12728265.
26. Bando SY, Andrade FB, Guth BEC, Elias WP, Moreira-Filho CA, Pestana de Castro AF. Atypical enteropathogenic Escherichia coli genomic background allows the acquisition of non-EPEC virulence factors. FEMS Microbiology Letters 2009, 299:22-30.
27. Bulgin R, Arbeloa A, Goulding D, Dougan G, Crepin VF, Raymond B, Frankel G. The T3SS effector EspT defines a new category of invasive enteropathogenic E. coli (EPEC) which form intracellular actin pedestals. PLoS Pathog 2009, 5(12):e1000683. 10.1371/journal.ppat.1000683, 2782363, 20011125.
28. Weflen AW, Alto NM, Viswanathan VK, Hecht G. E. coli secreted protein F promotes EPEC invasion of intestinal epithelial cells via an SNX9-dependent mechanism. Cell Microbiol 2010, 12:919-929. 10.1111/j.1462-5822.2010.01440.x, 20088948.
29. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature 2000, 405:299-304. 10.1038/35012500, 10830951.
30. Juhas M, van der Meer JR, Gaillard M, Harding RM, Hood DW, Crook DW. Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev 2009, 33:376-393. 10.1111/j.1574-6976.2008.00136.x, 2704930, 19178566.
31. Langille MGI, Brinkman FSL. IslandViewer: an integrated interface for computational identification and visualization of genomic islands. Bioinformatics 2009, 25:664-665. 10.1093/bioinformatics/btp030, 2647836, 19151094.
32. Nishino K, Inazumi Y, Yamaguchi A. Global analysis of genes regulated by EvgA of the two-component regulatory system in Escherichia coli. J Bacteriol 2003, 185:2667-2672. 10.1128/JB.185.8.2667-2672.2003, 152604, 12670992.
33. Devanathan S, Postle K. Studies on colicin B translocation: FepA is gated by TonB. Mol Microbiol 2007, 65:441-453. 10.1111/j.1365-2958.2007.05808.x, 17578453.
34. Fricke WF, McDermott PF, Mammel MK, Zhao S, Johnson TJ, Rasko DA, Fedorka-Cray PJ, Pedroso A, Whichard JM, Leclerc JE, et al. Antimicrobial resistance-conferring plasmids with similarity to virulence plasmids from avian pathogenic Escherichia coli strains in Salmonella enterica serovar Kentucky isolates from poultry. Applied and Environmental Microbiology 2009, 75:5963-5971. 10.1128/AEM.00786-09, 2747853, 19648374.
35. Tivendale KA, Noormohammadi AH, Allen JL, Browning GF. The conserved portion of the putative virulence region contributes to virulence of avian pathogenic Escherichia coli. Microbiology (Reading, Engl) 2009, 155:450-460.
36. Chen YT, Chang HY, Lai YC, Pan CC, Tsai SF, Peng HL. Sequencing and analysis of the large virulence plasmid pLVPK of Klebsiella pneumoniae CG43. Gene 2004, 337:189-198. 10.1016/j.gene.2004.05.008, 15276215.
37. Baichoo N, Helmann JD. Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J Bacteriol 2002, 184:5826-5832. 10.1128/JB.184.21.5826-5832.2002, 135393, 12374814.
38. Chen Z, Lewis KA, Shultzaberger RK, Lyakhov IG, Zheng M, Doan B, Storz G, Schneider TD. Discovery of Fur binding site clusters in Escherichia coli by information theory models. Nucleic Acids Res 2007, 35:6762-6777. 10.1093/nar/gkm631, 2189734, 17921503.
39. Mey AR, Wyckoff EE, Kanukurthy V, Fisher CR, Payne SM. Iron and fur regulation in Vibrio cholerae and the role of fur in virulence. Infect Immun 2005, 73:8167-8178. 10.1128/IAI.73.12.8167-8178.2005, 1307094, 16299312.
40. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA 2006, 103:1528-1533. 10.1073/pnas.0510322103, 1345711, 16432199.
41. Ma AT, McAuley S, Pukatzki S, Mekalanos JJ. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 2009, 5:234-243. 10.1016/j.chom.2009.02.005, 19286133.
42. Bingle LE, Bailey CM, Pallen MJ. Type VI secretion: a beginner's guide. Curr Opin Microbiol 2008, 11:3-8. 10.1016/j.mib.2008.01.006, 18289922.
43. Shrivastava S, Mande SS. Identification and functional characterization of gene components of Type VI Secretion system in bacterial genomes. PLoS ONE 2008, 3(8):e2955. 10.1371/journal.pone.0002955, 2492809, 18698408.
44. Plainvert C, Bidet P, Peigne C, Barbe V, Medigue C, Denamur E, Bingen E, Bonacorsi S. A new O-antigen gene cluster has a key role in the virulence of the Escherichia coli meningitis clone O45:K1:H7. J Bacteriol 2007, 189:8528-8536. 10.1128/JB.01013-07, 2168960, 17905975.
45. Pukatzki S, McAuley SB, Miyata ST. The type VI secretion system: translocation of effectors and effector-domains. Curr Opin Microbiol 2009, 12:11-17. 10.1016/j.mib.2008.11.010, 19162533.
46. Bringer MA, Barnich N, Glasser AL, Bardot O, Darfeuille-Michaud A. HtrA stress protein is involved in intramacrophagic replication of adherent and invasive Escherichia coli strain LF82 isolated from a patient with Crohn's disease. Infect Immun 2005, 73:712-721. 10.1128/IAI.73.2.712-721.2005, 546957, 15664909.
47. Barnich N, Bringer MA, Claret L, Darfeuille-Michaud A. Involvement of lipoprotein NlpI in the virulence of adherent invasive Escherichia coli strain LF82 isolated from a patient with Crohn's disease. Infect Immun 2004, 72:2484-2493. 10.1128/IAI.72.5.2484-2493.2004, 387872, 15102755.
48. Bringer MA, Rolhion N, Glasser AL, Darfeuille-Michaud A. The oxidoreductase DsbA plays a key role in the ability of the Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 to resist macrophage killing. J Bacteriol 2007, 189:4860-4871. 10.1128/JB.00233-07, 1913465, 17449627.
49. Rolhion N, Barnich N, Claret L, Darfeuille-Michaud A. Strong decrease in invasive ability and outer membrane vesicle release in Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 with the yfgL gene deleted. J Bacteriol 2005, 187:2286-2296. 10.1128/JB.187.7.2286-2296.2005, 1065249, 15774871.
50. Sachdeva G, Kumar K, Jain P, Ramachandran S. SPAAN: a software program for prediction of adhesins and adhesin-like proteins using neural networks. Bioinformatics 2005, 21:483-491. 10.1093/bioinformatics/bti028, 15374866.
51. Homeier T, Semmler T, Wieler LH, Ewers C. The GimA locus of extraintestinal pathogenic E. coli: does reductive evolution correlate with habitat and pathotype?. PLoS ONE 2010, 5(5):e10877. 10.1371/journal.pone.0010877, 2878320, 20526361.
52. Boudeau J, Barnich N, Darfeuille-Michaud A. Type 1 pili-mediated adherence of Escherichia coli strain LF82 isolated from Crohn's disease is involved in bacterial invasion of intestinal epithelial cells. Mol Microbiol 2001, 39:1272-1284. 10.1111/j.1365-2958.2001.02315.x, 11251843.
53. Sepehri S, Kotlowski R, Bernstein CN, Krause DO. Phylogenetic analysis of inflammatory bowel disease associated Escherichia coli and the fimH virulence determinant. Inflamm Bowel Dis 2009, 15:1737-1745. 10.1002/ibd.20966, 19462430.
54. Dorman CJ. Nucleoid-associated proteins and bacterial physiology. Adv Appl Microbiol 2009, 67:47-64. full_text, 19245936.
55. Fass E, Groisman EA. Control of Salmonella pathogenicity island-2 gene expression. Curr Opin Microbiol 2009, 12:199-204. 10.1016/j.mib.2009.01.004, 2805070, 19264535.
56. Yoon H, McDermott JE, Porwollik S, McClelland M, Heffron F. Coordinated regulation of virulence during systemic infection of Salmonella enterica serovar Typhimurium. PLoS Pathog 2009, 5(2):e1000306. 10.1371/journal.ppat.1000306, 2639726, 19229334.
57. Miquel S, Claret L, Bonnet R, Dorboz I, Barnich N, Darfeuille-Michaud A. Role of decreased levels of Fis histone-like protein in Crohn's disease-associated adherent invasive Escherichia coli LF82 bacteria interacting with intestinal epithelial cells. J Bacteriol 2010, 192:1832-1843. 10.1128/JB.01679-09, 2838056, 20118249.
58. Miethke M, Marahiel MA. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 2007, 71:413-451. 10.1128/MMBR.00012-07, 2168645, 17804665.
59. Hagan EC, Mobley HL. Uropathogenic Escherichia coli outer membrane antigens expressed during urinary tract infection. Infect Immun 2007, 75:3941-3949. 10.1128/IAI.00337-07, 1951972, 17517861.
60. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M, Pfeffer K, Russmann H, Hardt WD. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 2003, 71:2839-2858. 10.1128/IAI.71.5.2839-2858.2003, 153285, 12704158.
61. Strober W, Fuss I, Mannon P. The fundamental basis of inflammatory bowel disease. J Clin Invest 2007, 117:514-521. 10.1172/JCI30587, 1804356, 17332878.
62. Tomljenovic-Berube AM, Mulder DT, Whiteside MD, Brinkman FS, Coombes BK. Identification of the regulatory logic controlling Salmonella pathoadaptation by the SsrA-SsrB two-component system. PLoS Genet 2010, 6(3):e1000875. 10.1371/journal.pgen.1000875, 2837388, 20300643.
63. Osborne SE, Walthers D, Tomljenovic AM, Mulder DT, Silphaduang U, Duong N, Lowden MJ, Wickham ME, Waller RF, Kenney LJ, et al. Pathogenic adaptation of intracellular bacteria by rewiring a cis-regulatory input function. Proc Natl Acad Sci USA 2009, 106:3982-3987. 10.1073/pnas.0811669106, 2645909, 19234126.
64. Torres AG, Redford P, Welch RA, Payne SM. TonB-dependent systems of uropathogenic Escherichia coli: aerobactin and heme transport and TonB are required for virulence in the mouse. Infect Immun 2001, 69:6179-6185. 10.1128/IAI.69.10.6179-6185.2001, 98749, 11553558.
65. Kumar S, Nei M, Dudley J, Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinformatics 2008, 9:299-306. 10.1093/bib/bbn017, 2562624, 18417537.
66. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599. 10.1093/molbev/msm092, 17488738.
67. Welch RA, Burland V, Plunkett G, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J, et al. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 2002, 99:17020-17024. 10.1073/pnas.252529799, 139262, 12471157.
68. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Research 1999, 27:4636-4641. 10.1093/nar/27.23.4636, 148753, 10556321.
69. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. Journal of Molecular Biology 1990, 215:403-410.
70. Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, Fuellen G, Gilbert JGR, Korf I, Lapp H, et al. The Bioperl toolkit: Perl modules for the life sciences. Genome Research 2002, 12:1611-1618. 10.1101/gr.361602, 187536, 12368254.
71. Laing C, Buchanan C, Taboada EN, Zhang Y, Kropinski A, Villegas A, Thomas JE, Gannon VP. Pan-genome sequence analysis using Panseq: an online tool for the rapid analysis of core and accessory genomic regions. BMC Bioinformatics 2010, 11:461. 10.1186/1471-2105-11-461, 2949892, 20843356.
72. Koski LB, Gray MW, Lang BF, Burger G. AutoFACT: an automatic functional annotation and classification tool. BMC Bioinformatics 2005, 6:151. 10.1186/1471-2105-6-151, 1182349, 15960857.
73. Stothard P, Wishart DS. Circular genome visualization and exploration using CGView. Bioinformatics 2005, 21:537-539. 10.1093/bioinformatics/bti054, 15479716.
74. Grant JR, Stothard P. The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res 2008, 36:W181-184. 10.1093/nar/gkn179, 2447734, 18411202.
75. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. Circos: an information aesthetic for comparative genomics. Genome Research 2009, 19:1639-1645. 10.1101/gr.092759.109, 2752132, 19541911.
76. Moen ST, Blumentritt CA, Slater TM, Patel SD, Tutt CB, Estrella-Jimenez ME, Pawlik J, Sower L, Popov VL, Schein CH, et al. Testing the efficacy and toxicity of adenylyl cyclase inhibitors against enteric pathogens using in vitro and in vivo models of infection. Infect Immun 2010, 78:1740-1749. 10.1128/IAI.01114-09, 2849411, 20123712.
77. Arnow LE. Colorimetric determination of the components of 3,4-dihydroxyphenylalaninetyrosine mixtures. Journal of Biological Chemistry 1937, 118:531-537.
78. Atkin CL, Neilands JB, Phaff HJ. Rhodotorulic acid from species of Leucosporidium, Rhodosporidium, Rhodotorula, Sporidiobolus, and Sporobolomyces, and a new alanine-containing ferrichrome from Cryptococcus melibiosum. J Bacteriol 1970, 103:722-733. 248150, 5529038.
79. Miquel S, Peyretaillade E, Claret L, de Vallee A, Dossat C, Vacherie B, Zineb el H, Segurens B, Barbe V, Sauvanet P, et al. Complete genome sequence of Crohn's disease-associated adherent-invasive E. coli strain LF82. PLoS ONE 2010, 5(9). 10.1371/journal.pone.0012714, 2941450, 20862302.