Enhanced persistence in the colonic microbiota of Escherichia coli strains belonging to phylogenetic group B2: role of virulence factors and adherence to colonic cells.

Escherichia coli segregates into four phylogenetic groups, A, B1, B2 and D. B2 and D strains usually possess virulence factors, cause most extra-intestinal infections and have superior capacity to persist in the infantile colonic microbiota. Here, we investigated 24 resident and 37 transient E. coli strains from the colonic microbiota of 13 Swedish schoolgirls sampled in the 1970s with respect to phylogenetic group identity, carriage of virulence factor genes, O and K antigens and mannose-sensitive and -resistant adherence to the colonic cell line HT-29. Resident strains more often belonged to phylogenetic group B2 than transient strains (38% vs 5% p=0.004). In contrast, transient strains more often than resident strains belonged to group A (57% vs 29%, p=0.04) or B1 (24% vs 13%, p=0.33). Most B2 strains belonged to uropathogenic O serogroups, carried genes for P fimbriae, K5 capsule and hemolysin and adhered in higher numbers to HT-29 cells via mannose-resistant mechanisms than strains from the other groups. Further, among strains carrying genes for P or S fimbriae, those belonging to group B2 adhered in highest numbers. In logistic regression, genes for P fimbriae and aerobactin predicted persistence in the colonic microbiota (p=0.050 and 0.056, respectively), while B2 origin did not reach significance as an independent variable (p=0.16). Our results indicate that virulence factors carried by group B2 strains contribute to their strong colonizing capacity. These factors may actually be regarded as fitness factors in the human gut.

[1]  Jacques Elion,et al.  The Link between Phylogeny and Virulence inEscherichia coli Extraintestinal Infection , 1999, Infection and Immunity.

[2]  A. Siitonen,et al.  Quantitative differences in adhesiveness of type 1 fimbriated Escherichia coli due to structural differences in fimH genes , 1995, Journal of bacteriology.

[3]  S. Hull,et al.  Attachment of Escherichia coli via mannose- or Gal alpha 1----4Gal beta-containing receptors to human colonic epithelial cells , 1988, Infection and immunity.

[4]  Cooke Em,et al.  Properties of Strains of Escherichia Coli Isolated from a Variety of Sources , 1975 .

[5]  D. Caugant,et al.  Resident colonic Escherichia coli strains frequently display uropathogenic characteristics. , 1992, The Journal of infectious diseases.

[6]  O. Clermont,et al.  The Yersinia high-pathogenicity island is highly predominant in virulence-associated phylogenetic groups of Escherichia coli. , 2001, FEMS microbiology letters.

[7]  F. Nowrouzian,et al.  Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants. , 2005, The Journal of infectious diseases.

[8]  W. R. Mccabe,et al.  Escherichia coli in bacteremia: K and O antigens and serum sensitivity of strains from adults and neonates. , 1978, The Journal of infectious diseases.

[9]  B. Levin,et al.  Genetic diversity and structure in Escherichia coli populations. , 1980, Science.

[10]  S. Hultgren,et al.  Binding of Pili from UropathogenicEscherichia coli to Membranes Secreted by Human Colonocytes and Enterocytes , 1999, Infection and Immunity.

[11]  H J SEARS,et al.  FURTHER OBSERVATIONS ON THE PERSISTENCE OF INDIVIDUAL STRAINS OF ESCHERICHIA COLI IN THE INTESTINAL TRACT OF MAN , 1952, Journal of bacteriology.

[12]  E. Falsen,et al.  Characteristics of antibiotic-resistant Escherichia coli in the rectum of healthy school-children. , 1977, Journal of medical microbiology.

[13]  M. Kuskowski,et al.  Phylogenetic distribution of virulence-associated genes among Escherichia coli isolates associated with neonatal bacterial meningitis in the Netherlands. , 2002, The Journal of infectious diseases.

[14]  F. Nowrouzian,et al.  P fimbriae and aerobactin as intestinal colonization factors for Escherichia coli in Pakistani infants , 2001, Epidemiology and Infection.

[15]  H. J. Sears,et al.  PERSISTENCE OF INDIVIDUAL STRAINS OF ESCHERICHIA COLI IN MAN AND DOG UNDER VARYING CONDITIONS , 1956, Journal of bacteriology.

[16]  M. Kuskowski,et al.  Phylogenetic origin and virulence genotype in relation to resistance to fluoroquinolones and/or extended-spectrum cephalosporins and cephamycins among Escherichia coli isolates from animals and humans. , 2003, The Journal of infectious diseases.

[17]  I. Ørskov,et al.  Summary of a Workshop on the Clone Concept in the Epidemiology, Taxonomy, and Evolution of the Enterobacteriaceae and other Bacteria , 1983 .

[18]  R. Gillies,et al.  Fimbriæ and adhesive properties in dysentery bacilli , 1957 .

[19]  O. Clermont,et al.  Rapid and Simple Determination of theEscherichia coli Phylogenetic Group , 2000, Applied and Environmental Microbiology.

[20]  S. Hultgren,et al.  Role of intestinal surfactant-like particles as a potential reservoir of uropathogenic Escherichia coli. , 2000, Biochimica et biophysica acta.

[21]  E. Denamur,et al.  Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. , 2001, Microbiology.

[22]  A. Cross,et al.  The biologic significance of bacterial encapsulation. , 1990, Current topics in microbiology and immunology.

[23]  H J SEARS,et al.  PERSISTENCE OF INDIVIDUAL STRAINS OF ESCHERICHIA COLI IN THE INTESTINAL TRACT OF MAN , 1950, Journal of bacteriology.

[24]  D. Hartl,et al.  Chromosomal Regions Specific to Pathogenic Isolates of Escherichia coli Have a Phylogenetically Clustered Distribution , 1998, Journal of bacteriology.

[25]  T. Midtvedt,et al.  Role of Escherichia coli P fimbriae in intestinal colonization in gnotobiotic rats , 1995, Infection and immunity.

[26]  S. Inouye,et al.  Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli , 1990, Journal of bacteriology.

[27]  C. Svanborg,et al.  P fimbriae and other adhesins enhance intestinal persistence of Escherichia coli in early infancy , 1998, Epidemiology and Infection.

[28]  B. Picard,et al.  Highly pathogenic strains of Escherichia coli revealed by the distinct electrophoretic patterns of carboxylesterase B. , 1986, Journal of general microbiology.

[29]  J. Heesemann,et al.  Prevalence of the “High-Pathogenicity Island” of Yersinia Species among Escherichia coliStrains That Are Pathogenic to Humans , 1998, Infection and Immunity.

[30]  E. Cooke,et al.  Hospital food as a possible source of Escherichia coli in patients. , 1970, Lancet.

[31]  A. Stams,et al.  Purification and some properties of the methyl-CoM reductase of Methanothrix soehngenii , 1990 .

[32]  B. Picard,et al.  Characterization of highly virulent Escherichia coli strains by ribosomal DNA restriction fragment length polymorphism. , 1991, FEMS microbiology letters.

[33]  B. Picard,et al.  Comparative esterase electrophoretic polymorphism of Escherichia coli isolates obtained from animal and human sources. , 1986, Journal of general microbiology.

[34]  I. Strannegård,et al.  Escherichia coli in Infants' Intestinal Microflora: Colonization Rate, Strain Turnover, and Virulence Gene Carriage , 2003, Pediatric Research.

[35]  C. Svanborg,et al.  Adhesins of Escherichia coli associated with extra-intestinal pathogenicity confer binding to colonic epithelial cells. , 1995, Microbial Pathogenesis.

[36]  E. Denamur,et al.  The FimH A27V Mutation Is Pathoadaptive for Urovirulence in Escherichia coli B2 Phylogenetic Group Isolates , 2003, Infection and Immunity.

[37]  B. Foxman,et al.  Both Urinary and Rectal Escherichia coli Isolates Are Dominated by Strains of Phylogenetic Group B2 , 2002, Journal of Clinical Microbiology.

[38]  B. Kaijser Immunology of Escherichia coli: K antigen and its relation to urinary-tract infection. , 1973, The Journal of infectious diseases.

[39]  K. Bettelheim,et al.  A study of Escherichia coli isolated from chronic urinary infection. , 1969, Journal of medical microbiology.

[40]  F. Nowrouzian,et al.  P fimbriae, capsule and aerobactin characterize colonic resident Escherichia coli , 2001, Epidemiology and Infection.

[41]  J. R. Johnson,et al.  Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. , 2000, The Journal of infectious diseases.