F9 fimbriae of uropathogenic Escherichia coli are expressed at low temperature and recognise Galb1-3GlcNAc-containing glycans

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Wurpel, Daniël J ^a   Totsika, Makrina ^a   Allsopp, Luke P ^a   Hartley Tassell, Lauren E ^b   Day, Christopher J ^b   Peters, Kate M ^a   Sarkar, Sohinee ^a   Ulett, Glen C ^b   Yang, Ji ^c   Tiralongo, Joe ^b   Strugnell, Richard A ^c   Jennings, Michael P ^b   Schembri, Mark A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; GLYCAN; HISTONE LIKE NUCLEOID STRUCTURING PROTEIN; ESCHERICHIA COLI PROTEIN; GALACTOSE; N ACETYLGLUCOSAMINE; POLYSACCHARIDE;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BIOFILM; CONTROLLED STUDY; F9 GENE; FIMBRIA; GENE REPRESSION; LOW TEMPERATURE; NONHUMAN; OPERON; PROMOTER REGION; UROPATHOGENIC ESCHERICHIA COLI; AMINO ACID SEQUENCE; BACTERIUM ADHERENCE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY;

ACETYLGLUCOSAMINE; ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; BACTERIAL ADHESION; BASE SEQUENCE; BIOFILMS; ESCHERICHIA COLI PROTEINS; EVOLUTION, MOLECULAR; FIMBRIAE, BACTERIAL; GALACTOSE; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MOLECULAR SEQUENCE DATA; OPERON; PHYLOGENY; POLYSACCHARIDES; TRANSCRIPTION, GENETIC; UROPATHOGENIC ESCHERICHIA COLI;

EID: 84899867671     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093177     Document Type: Article

References (88)

1. Foxman B (2002) Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am J Med 113 Suppl 1A: 5S-13S.
2. Stamm WE (1991) Catheter-associated urinary tract infections: epidemiology, pathogenesis, and prevention. Am J Med 91: 65S-71S.
3. Klemm P, Schembri MA (2000) Bacterial adhesins: function and structure. Int J Med Microbiol 290: 27-35. (Pubitemid 30217988)
4. Oelschlaeger TA, Dobrindt U, Hacker J (2002) Virulence factors of uropathogens. Curr Opin Urol 12: 33-38. (Pubitemid 34033066)
5. Hahn E, Wild P, Hermanns U, Sebbel P, Glockshuber R, et al. (2002) Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J Mol Biol 323: 845-857. (Pubitemid 35341059)
6. Jones CH, Pinkner JS, Roth R, Heuser J, Nicholes AV, et al. (1995) FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. Proc Natl Acad Sci U S A 92: 2081-2085.
7. Nilsson P, Uhlin BE (1991) Differential decay of a polycistronic Escherichia coli transcript is initiated by RNaseE-dependent endonucleolytic processing. Mol Microbiol 5: 1791-1799. (Pubitemid 21896210)
8. Wurpel DJ, Beatson SA, Totsika M, Petty NK, Schembri MA (2013) Chaperone-Usher Fimbriae of Escherichia coli. PloS one 8: e52835.
9. Waksman G, Hultgren SJ (2009) Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol 7: 765-774.
10. Wu XR, Sun TT, Medina JJ (1996) In vitro binding of type 1-fimbriated Escherichia coli to uroplakins Ia and Ib: relation to urinary tract infections. Proc Natl Acad Sci U S A 93: 9630-9635.
11. Leffler H, Svanborg-Eden C (1981) Glycolipid receptors for uropathogenic Escherichia coli on human erythrocytes and uroepithelial cells. Infect Immun 34: 920-929.
12. Kallenius G, Mollby R, Svenson SB, Helin I, Hultberg H, et al. (1981) Occurrence of P-fimbriated Escherichia coli in urinary tract infections. Lancet 2: 1369-1372. (Pubitemid 12239441)
13. Khan AS, Kniep B, Oelschlaeger TA, Van Die I, Korhonen T, et al. (2000) Receptor structure for F1C fimbriae of uropathogenic Escherichia coli. Infect Immun 68: 3541-3547. (Pubitemid 30340455)
14. Korhonen TK, Parkkinen J, Hacker J, Finne J, Pere A, et al. (1986) Binding of Escherichia coli S fimbriae to human kidney epithelium. Infect Immun 54: 322-327. (Pubitemid 17171439)
15. Marre R, Kreft B, Hacker J (1990) Genetically engineered S and F1C fimbriae differ in their contribution to adherence of Escherichia coli to cultured renal tubular cells. Infect Immun 58: 3434-3437. (Pubitemid 20293458)
16. Ulett GC, Mabbett AN, Fung KC, Webb RI, Schembri MA (2007) The role of F9 fimbriae of uropathogenic Escherichia coli in biofilm formation. Microbiology 153: 2321-2331. (Pubitemid 47074085)
17. Nuccio SP, Baumler AJ (2007) Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 71: 551-575.
18. Low AS, Dziva F, Torres AG, Martinez JL, Rosser T, et al. (2006) Cloning, expression, and characterization of fimbrial operon F9 from enterohemorrhagic Escherichia coli O157:H7. Infect Immun 74: 2233-2244.
19. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402. (Pubitemid 27359211)
20. Sullivan MJ, Petty NK, Beatson SA (2011) Easyfig: a genome comparison visualizer. Bioinformatics 27: 1009-1010.
21. Wirth T, Falush D, Lan R, Colles F, Mensa P, et al. (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60: 1136-1151.
22. Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23: 127-128. (Pubitemid 46017867)
23. Mobley HL, Green DM, Trifillis AL, Johnson DE, Chippendale GR, et al. (1990) Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun 58: 1281-1289. (Pubitemid 20151789)
24. Bertani G (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62: 293-300.
25. Cormack BP, Valdivia RH, Falkow S (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173: 33-38. (Pubitemid 26239677)
26. 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. (Pubitemid 30412767)
27. Murphy TF, Loeb MR (1989) Isolation of the outer membrane of Branhamella catarrhalis. Microb Pathog 6: 159-174. (Pubitemid 19139556)
28. (2005) Rapid amplification of 5′ complementary DNA ends (59 RACE). Nat Methods 2: 629-630.
29. Beloin C, Dorman C (2003) An extended role for the nucleoid structuring protein H-NS in the virulence gene regulatory cascade of Shigella flexneri. Molecular Microbiology 47: 825-838. (Pubitemid 36114988)
30. Schembri MA, Klemm P (2001) Biofilm formation in a hydrodynamic environment by novel fimh variants and ramifications for virulence. Infect Immun 69: 1322-1328. (Pubitemid 32187576)
31. Day CJ, Tiralongo J, Hartnell RD, Logue CA, Wilson JC, et al. (2009) Differential carbohydrate recognition by Campylobacter jejuni strain 11168: influences of temperature and growth conditions. PLoS One 4: e4927.
32. Alvarez RA, Blixt O (2006) Identification of ligand specificities for glycan-binding proteins using glycan arrays. Methods Enzymol 415: 292-310. (Pubitemid 44751104)
33. Allsopp LP, Beloin C, Ulett GC, Valle J, Totsika M, et al. (2012) Molecular characterization of UpaB and UpaC, two new autotransporter proteins of uropathogenic Escherichia coli CFT073. Infect Immun 80: 321-332.
34. Korea CG, Badouraly R, Prevost MC, Ghigo JM, Beloin C (2010) Escherichia coli K-12 possesses multiple cryptic but functional chaperone-usher fimbriae with distinct surface specificities. Environ Microbiol 12: 1957-1977.
35. Grote A, Klein J, Retter I, Haddad I, Behling S, et al. (2009) PRODORIC (release 2009): a database and tool platform for the analysis of gene regulation in prokaryotes. Nucleic Acids Res 37: D61-65.
36. Amit R, Oppenheim AB, Stavans J (2003) Increased bending rigidity of single DNA molecules by H-NS, a temperature and osmolarity sensor. Biophys J 84: 2467-2473. (Pubitemid 36373568)
37. Ono S, Goldberg MD, Olsson T, Esposito D, Hinton JC, et al. (2005) H-NS is a part of a thermally controlled mechanism for bacterial gene regulation. Biochem J 391: 203-213. (Pubitemid 41532416)
38. Easton DM, Totsika M, Allsopp LP, Phan MD, Idris A, et al. (2011) Characterization of EhaJ, a New Autotransporter Protein from Enterohemorrhagic and Enteropathogenic Escherichia coli. Front Microbiol 2: 120.
39. 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. (Pubitemid 39545311)
40. van Diemen PM, Dziva F, Stevens MP, Wallis TS (2005) Identification of enterohemorrhagic Escherichia coli O26:H- genes required for intestinal colonization in calves. Infect Immun 73: 1735-1743. (Pubitemid 40470762)
41. Dorman CJ (2007) H-NS, the genome sentinel. Nat Rev Microbiol 5: 157-161.
42. Muller CM, Dobrindt U, Nagy G, Emody L, Uhlin BE, et al. (2006) Role of histone-like proteins H-NS and StpA in expression of virulence determinants of uropathogenic Escherichia coli. J Bacteriol 188: 5428-5438. (Pubitemid 44157299)
43. Totsika M, Wells TJ, Beloin C, Valle J, Allsopp LP, et al. (2012) Molecular characterization of the EhaG and UpaG trimeric autotransporter proteins from pathogenic Escherichia coli. Appl Environ Microbiol 78: 2179-2189.
44. Rendon MA, Saldana Z, Erdem AL, Monteiro-Neto V, Vazquez A, et al. (2007) Commensal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization. Proc Natl Acad Sci U S A 104: 10637-10642. (Pubitemid 47185717)
45. Pouttu R, Westerlund-Wikstrom B, Lang H, Alsti K, Virkola R, et al. (2001) matB, a common fimbrillin gene of Escherichia coli, expressed in a genetically conserved, virulent clonal group. J Bacteriol 183: 4727-4736. (Pubitemid 32708957)
46. Lehti TA, Bauchart P, Kukkonen M, Dobrindt U, Korhonen TK, et al. (2013) Phylogenetic group-associated differences in regulation of the common colonization factor Mat fimbria in Escherichia coli. Mol Microbiol.
47. Garnett JA, Martinez-Santos VI, Saldana Z, Pape T, Hawthorne W, et al. (2012) Structural insights into the biogenesis and biofilm formation by the Escherichia coli common pilus. Proc Natl Acad Sci U S A 109: 3950-3955.
48. Olsen A, Jonsson A, Normark S (1989) Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338: 652-655. (Pubitemid 19104644)
49. Stromberg N, Marklund BI, Lund B, Ilver D, Hamers A, et al. (1990) Host-specificity of uropathogenic Escherichia coli depends on differences in binding specificity to Gal alpha 1-4Gal-containing isoreceptors. Embo J 9: 2001-2010.
50. Stahl B, Thurl S, Zeng J, Karas M, Hillenkamp F, et al. (1994) Oligosaccharides from human milk as revealed by matrix-assisted laser desorption/ionization mass spectrometry. Anal Biochem 223: 218-226. (Pubitemid 24368970)
51. Teneberg S, Leonardsson I, Karlsson H, Jovall PA, Angstrom J, et al. (2002) Lactotetraosylceramide, a novel glycosphingolipid receptor for Helicobacter pylori, present in human gastric epithelium. J Biol Chem 277: 19709-19719. (Pubitemid 34975643)
52. Welch RA, Burland V, Plunkett G 3rd, Redford P, Roesch P, et al. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 99: 17020-17024. (Pubitemid 36034091)
53. Kjaergaard K, Schembri MA, Ramos C, Molin S, Klemm P (2000) Antigen 43 facilitates formation of multispecies biofilms. Environ Microbiol 2: 695-702. (Pubitemid 33136684)
54. Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
55. Bolivar F, Rodriguez RL, Greene PJ, Betlach MC, Heyneker HL, et al. (1977) Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2: 95-113. (Pubitemid 9021046)
56. Chang AC, Cohen SN (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141-1156. (Pubitemid 8354538)
57. Avasthi TS, Kumar N, Baddam R, Hussain A, Nandanwar N, et al. (2011) Genome of multidrug-resistant uropathogenic Escherichia coli strain NA114 from India. J Bacteriol 193: 4272-4273.
58. Chen SL, Hung CS, Xu J, Reigstad CS, Magrini V, et al. (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.
59. Hochhut B,Wilde C, Balling G, Middendorf B, Dobrindt U, et al. (2006) Role of pathogenicity island-associated integrases in the genome plasticity of uropathogenic Escherichia coli strain 536. Mol Microbiol 61: 584-595. (Pubitemid 44324086)
60. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, et al. (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5: e1000344.
61. Zdziarski J, Brzuszkiewicz E, Wullt B, Liesegang H, Biran D, et al. (2010) Host imprints on bacterial genomes - rapid, divergent evolution in individual patients. PLoS Pathog 6: e1001078.
62. Moriel DG, Bertoldi I, Spagnuolo A, Marchi S, Rosini R, et al. (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.
63. Lu S, Zhang X, Zhu Y, Kim KS, Yang J, et al. (2011) Complete genome sequence of the neonatal-meningitis-associated Escherichia coli strain CE10. J Bacteriol 193: 7005.
64. Johnson TJ, Kariyawasam S, Wannemuehler Y, Mangiamele P, Johnson SJ, et al. (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. (Pubitemid 46697413)
65. Miquel S, Claret L, Bonnet R, Dorboz I, Barnich N, et al. (2010) 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 192: 1832-1843.
66. Nash JH, Villegas A, Kropinski AM, Aguilar-Valenzuela R, Konczy P, et al. (2010) Genome sequence of adherent-invasive Escherichia coli and comparative genomic analysis with other E. coli pathotypes. BMC Genomics 11: 667.
67. Krause DO, Little AC, Dowd SE, Bernstein CN (2011) Complete genome sequence of adherent invasive Escherichia coli UM146 isolated from Ileal Crohn's disease biopsy tissue. J Bacteriol 193: 583.
68. Chaudhuri RR, Sebaihia M, Hobman JL, Webber MA, Leyton DL, et al. (2010) Complete genome sequence and comparative metabolic profiling of the prototypical enteroaggregative Escherichia coli strain 042. PLoS One 5: e8801.
69. Iguchi A, Thomson NR, Ogura Y, Saunders D, Ooka T, et al. (2009) Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J Bacteriol 191: 347-354.
70. Zhou Z, Li X, Liu B, Beutin L, Xu J, et al. (2010) Derivation of Escherichia coli O157:H7 from its O55:H7 precursor. PLoS One 5: e8700.
71. Kyle JL, Cummings CA, Parker CT, Quinones B, Vatta P, et al. (2012) Escherichia coli serotype O55:H7 diversity supports parallel acquisition of bacteriophage at Shiga toxin phage insertion sites during evolution of the O157:H7 lineage. J Bacteriol 194: 1885-1896.
72. Crossman LC, Chaudhuri RR, Beatson SA, Wells TJ, Desvaux M, et al. (2010) A commensal gone bad: complete genome sequence of the prototypical enterotoxigenic Escherichia coli strain H10407. J Bacteriol 192: 5822-5831.
73. Rasko DA, Rosovitz MJ, Myers GS, Mongodin EF, Fricke WF, et al. (2008) The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190: 6881-6893.
74. Ogura Y, Ooka T, Iguchi A, Toh H, Asadulghani M, et al. (2009) Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proc Natl Acad Sci U S A 106: 17939-17944.
75. Perna NT, Plunkett G 3rd, Burland V, Mau B, Glasner JD, et al. (2001) Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409: 529-533. (Pubitemid 32144360)
76. Hayashi T, Makino K, Ohnishi M, Kurokawa K, Ishii K, et al. (2001) Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res 8: 11-22. (Pubitemid 33617542)
77. Eppinger M, Mammel MK, Leclerc JE, Ravel J, Cebula TA (2011) Genomic anatomy of Escherichia coli O157:H7 outbreaks. Proc Natl Acad Sci U S A 108: 20142-20147.
78. Kulasekara BR, Jacobs M, Zhou Y, Wu Z, Sims E, et al. (2009) Analysis of the genome of the Escherichia coli O157:H7 2006 spinach-associated outbreak isolate indicates candidate genes that may enhance virulence. Infect Immun 77: 3713-3721.
79. Xiong Y, Wang P, Lan R, Ye C, Wang H, et al. (2012) A novel Escherichia coli O157:H7 clone causing a major hemolytic uremic syndrome outbreak in China. PLoS One 7: e36144.
80. Fricke WF, Wright MS, Lindell AH, Harkins DM, Baker-Austin C, et al. (2008) Insights into the environmental resistance gene pool from the genome sequence of the multidrug-resistant environmental isolate Escherichia coli SMS-3-5. J Bacteriol 190: 6779-6794.
81. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, et al. (2012) The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40: D26-32.
82. Oshima K, Toh H, Ogura Y, Sasamoto H, Morita H, et al. (2008) Complete genome sequence and comparative analysis of the wild-type commensal Escherichia coli strain SE11 isolated from a healthy adult. DNA Res 15: 375-386.
83. Archer CT, Kim JF, Jeong H, Park JH, Vickers CE, et al. (2011) The genome sequence of E. coli W (ATCC 9637): comparative genome analysis and an improved genome-scale reconstruction of E. coli. BMC Genomics 12: 9.
84. Toh H, Oshima K, Toyoda A, Ogura Y, Ooka T, et al. (2010) Complete genome sequence of the wild-type commensal Escherichia coli strain SE15, belonging to phylogenetic group B2. J Bacteriol 192: 1165-1166.
85. Jeong H, Barbe V, Lee CH, Vallenet D, Yu DS, et al. (2009) Genome sequences of Escherichia coli B strains REL606 and BL21(DE3). J Mol Biol 394: 644-652.
86. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1462. (Pubitemid 27449228)
87. Durfee T, Nelson R, Baldwin S, Plunkett G 3rd, Burland V, et al. (2008) The complete genome sequence of Escherichia coli DH10B: insights into the biology of a laboratory workhorse. J Bacteriol 190: 2597-2606. (Pubitemid 351466356)
88. Ferenci T, Zhou Z, Betteridge T, Ren Y, Liu Y, et al. (2009) Genomic sequencing reveals regulatory mutations and recombinational events in the widely used MC4100 lineage of Escherichia coli K-12. J Bacteriol 191: 4025-4029.