Identification and mechanism of evolution of new alleles coding for the AIDA-I autotransporter of porcine pathogenic Escherichia coli

Applied and Environmental Microbiology

Volumn 78, Issue 13, 2012, Pages 4597-4605

  Côté, Jean Philippe ^a   Berthiaume, Frédéric ^a   Houle, Sébastien ^b   Fairbrother, John M ^a   Dozois, Charles M ^b   Mourez, Michael ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PATHOGENS; DIFFUSE ADHERENCE; ELECTROPHORESIS ANALYSIS; EPITHELIAL CELLS; GENETIC RECOMBINATIONS; GLYCOSYLATED; HIGH MOLECULAR WEIGHT; OUTER MEMBRANE PROTEIN; PATHOGENIC ESCHERICHIA COLI; VIRULENCE FACTORS;

BIOLOGICAL MEMBRANES; ELECTROPHORESIS; ESCHERICHIA COLI;

GENES;

ADHESIN; AIDA I PROTEIN, E COLI; AIDA-I PROTEIN, E COLI; AUTOTRANSPORTER ADHESIN HEPTOSYLTRANSFERASE, E COLI; AUTOTRANSPORTER-ADHESIN-HEPTOSYLTRANSFERASE, E COLI; BACTERIAL DNA; ESCHERICHIA COLI PROTEIN; GLYCOSYLTRANSFERASE; VIRULENCE FACTOR;

ALLELE; COLIFORM BACTERIUM; DISEASE TRANSMISSION; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENETICS; IDENTIFICATION METHOD; PATHOGEN; PHYLOGENETICS; PIG; PLASMID; PROTEIN; VIRULENCE;

ALLELE; ANIMAL; ANIMAL DISEASE; ARTICLE; CHEMISTRY; CLUSTER ANALYSIS; DNA SEQUENCE; DNA SHUFFLING; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOLECULAR TYPING; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYLOGENY; PLASMID; PULSED FIELD GEL ELECTROPHORESIS; SWINE; SWINE DISEASE;

ADHESINS, ESCHERICHIA COLI; ALLELES; ANIMALS; CLUSTER ANALYSIS; DNA SHUFFLING; DNA, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; EVOLUTION, MOLECULAR; GLYCOSYLTRANSFERASES; MOLECULAR SEQUENCE DATA; MOLECULAR TYPING; PHYLOGENY; PLASMIDS; SEQUENCE ANALYSIS, DNA; SWINE; SWINE DISEASES; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; SUIDAE; SUS;

EID: 84864096615     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00906-12     Document Type: Article

References (37)

1. Benz I, Schmidt MA. 1989. Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect. Immun. 57:1506-1511.
2. Benz I, Schmidt MA. 2001. Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol. Microbiol. 40:1403-1413
3. Benz I, van Alen T, Bolte J, Wormann ME, Schmidt MA. 2010. Modulation of transcription and characterization of the promoter organization of the autotransporter adhesin heptosyltransferase and the autotransporter adhesin AIDA-I. Microbiology 156:1155-1166.
4. Berthiaume F, Leblond MF, Harel J, Mourez M. 2010. Growth-phasedependent expression of the operon coding for the glycosylated autotransporter adhesin AIDA-I of pathogenic Escherichia coli. FEMS Microbiol. Lett. 311:176-184.
5. Brockmeyer J, et al. 2007. Subtypes of the plasmid-encoded serine protease EspP in Shiga toxin-producing Escherichia coli: distribution, secretion, and proteolytic activity. Appl. Environ. Microbiol. 73:6351-6359.
6. Bruant G, et al. 2009. Two distinct groups of porcine enteropathogenic Escherichia coli strains of serogroup O45 are revealed by comparative genomic hybridization and virulence gene microarray. BMC Genomics 10:402. doi:10.1186/1471-2164-10-402.
7. Charbonneau ME, Berthiaume F, Mourez M. 2006. Proteolytic processing is not essential for multiple functions of the Escherichia coli autotransporter adhesin involved in diffuse adherence (AIDA-I). J. Bacteriol. 188: 8504-8512.
8. Charbonneau ME, et al. 2007. O-linked glycosylation ensures the normal conformation of the autotransporter adhesin involved in diffuse adherence. J. Bacteriol. 189:8880-8889.
9. Charbonneau ME, Janvore J, Mourez M. 2009. Autoprocessing of the Escherichia coli AIDA-I autotransporter: a new mechanism involving acidic residues in the junction region. J. Biol. Chem. 284:17340-17351.
10. Charbonneau ME, Mourez M. 2007. Functional organization of the autotransporter adhesin involved in diffuse adherence. J. Bacteriol. 189: 9020-9029.
11. Chomczynski P. 1992. One-hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal. Biochem. 201:134-139.
12. Clinical and Laboratory Standards Institute. 2008. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; approved standard. CLSI document M31-3, 3rd ed. Clinical and Laboratory Standards Institute, Wayne, PA.
13. Dautin N, Bernstein HD. 2007. Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol. 61:89-112.
14. Dubreuil JD. 2010. STb and AIDA-I: the missing link? Crit. Rev. Microbiol. 36:212-220.
15. Girard V, et al. 2010. Conformation change in a self-recognizing autotransporter modulates bacterial cell-cell interaction. J. Biol. Chem. 285: 10616-10626.
16. Henderson IR, Meehan M, Owen P. 1997. Antigen 43, a phase-variable bipartite outer membrane protein, determines colony morphology and autoaggregation in Escherichia coli K-12. FEMS Microbiol. Lett. 149:115-120.
17. Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC, Ala'Aldeen D. 2004. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
18. Jallat C, Livrelli V, Darfeuille-Michaud A, Rich C, Joly B. 1993. Escherichia coli strains involved in diarrhea in France: high prevalence and heterogeneity of diffusely adhering strains. J. Clin. Microbiol. 31:2031-2037.
19. Johnson TJ, et al. 2010. Pyrosequencing of the Vir plasmid of necrotoxigenic Escherichia coli. Vet. Microbiol. 144:100-109.
20. Kado CI, Liu ST. 1981. Rapid procedure for detection and isolation of large and small plasmids. J. Bacteriol. 145:1365-1373.
21. Klemm P, Hjerrild L, Gjermansen M, Schembri MA. 2004. Structurefunction analysis of the self-recognizing antigen 43 autotransporter protein from Escherichia coli. Mol. Microbiol. 51:283-296.
22. Klemm P, Vejborg RM, Sherlock O. 2006. Self-associating autotransporters, SAATs: functional and structural similarities. Int. J. Med. Microbiol. 296:187-195.
23. Lindenthal C, Elsinghorst EA. 1999. Identification of a glycoprotein produced by enterotoxigenic Escherichia coli. Infect. Immun. 67:4084-4091.
24. Mainil JG, Jacquemin E, Pohl P, Kaeckenbeeck A, Benz I. 2002. DNA sequences coding for the F18 fimbriae and AIDA adhesin are localised on the same plasmid in Escherichia coli isolates from piglets. Vet. Microbiol. 86:303-311.
25. Nagy B, Casey TA, Whipp SC, Moon HW. 1992. Susceptibility of porcine intestine to pilus-mediated adhesion by some isolates of piliated enterotoxigenic Escherichia coli increases with age. Infect. Immun. 60: 1285-1294.
26. Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
27. Nataro JP, et al. 1987. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr. Infect. Dis. J. 6:829-831.
28. Ngeleka M, Pritchard J, Appleyard G, Middleton DM, Fairbrother JM. 2003. Isolation and association of Escherichia coli AIDA-I/STb, rather than EAST1 pathotype, with diarrhea in piglets and antibiotic sensitivity of isolates. J. Vet. Diagn. Invest. 15:242-252.
29. Niewerth U, et al. 2001. The AIDA autotransporter system is associated with F18 and stx2e in Escherichia coli isolates from pigs diagnosed with edema disease and postweaning diarrhea. Clin. Diagn. Lab. Immunol. 8:143-149.
30. Oliver DC, Huang G, Nodel E, Pleasance S, Fernandez RC. 2003. A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol. Microbiol. 47:1367-1383.
31. Ravi M, et al. 2007. Contribution of AIDA-I to the pathogenicity of a porcine diarrheagenic Escherichia coli and to intestinal colonization through biofilm formation in pigs. Vet. Microbiol. 120:308-319.
32. Renn JP, Clark PL. 2008. A conserved stable core structure in the passenger domain beta-helix of autotransporter virulence proteins. Biopolymers 89:420-427.
33. Restieri C, Garriss G, Locas MC, Dozois CM. 2007. Autotransporterencoding sequences are phylogenetically distributed among Escherichia coli clinical isolates and reference strains. Appl. Environ. Microbiol. 73: 1553-1562.
34. Taillon C, Nadeau E, Mourez M, Dubreuil JD. 2008. Heterogeneity of Escherichia coli STb enterotoxin isolated from diseased pigs. J. Med. Microbiol. 57:887-890.
35. van der Woude MW, Henderson IR. 2008. Regulation and function of Ag43 (flu). Annu. Rev. Microbiol. 62:153-169.
36. Zhang W, Zhao M, Ruesch L, Omot A, Francis D. 2007. Prevalence of virulence genes in Escherichia coli strains recently isolated from young pigs with diarrhea in the US. Vet. Microbiol. 123:145-152.
37. Zhao L, Chen X, Xu X, Song G, Liu X. 2009. Analysis of the AIDA-I gene sequence and prevalence in Escherichia coli isolates from pigs with postweaning diarrhoea and oedema disease. Vet. J. 180:124-129.