Escherichia coli B2 Phylogenetic Subgroups in the Infant Gut Microbiota: Predominance of Uropathogenic Lineages in Swedish Infants and Enteropathogenic Lineages in Pakistani Infants

Abstract

Escherichia coli segregates into phylogenetic groups, with group B2 containing both extraintestinal pathogenic E. coli (ExPEC) and enteropathogenic E. coli (EPEC) strains. Ten main B2 subgroups (subgroups I to X)/sequence type complexes (STcs), as well as EPEC lineages, have been identified. In the current study, we characterized ExPEC and EPEC strains of E. coli B2 phylogenetic subgroups/STcs that colonize Swedish and Pakistani infants. Gut commensal E. coli B2 strains, 120 from Swedish infants (n = 87) and 19 from Pakistani infants (n = 12), were assigned to B2 subgroups. Carriage of the bundle-forming pili and intimin adhesin was examined in the EPEC lineages. The ExPEC virulence markers and the time of persistence of the strains in the microbiota were previously determined. In total, 84% of the Swedish strains and 47% of the Pakistani strains belonged to 1 of the 10 main B2 subgroups (P = 0.001). Among the Swedish strains, the most common B2 subgroups were IX/STc95 (19%), II/STc73 (17%), VI/STc12 (13%), and III/STc127 (11%), with each subgroup carrying distinctive sets of ExPEC virulence markers. EPEC lineages with few ExPEC features constituted 47% of the Pakistani B2 strains but only 7% of the Swedish B2 strains (P = 0.0001). The subgroup distribution within phylogenetic group B2 strains colonizing the gut differed between Swedish and Pakistani infants. B2 subgroups with uropathogenic characteristics dominated the gut microbiota of Swedish infants, while EPEC lineage 1 strains frequently colonized the intestines of Pakistani infants. Moreover, within the B2 subgroups, ExPEC virulence genes were more prevalent in Swedish strains than in Pakistani strains. Thus, ExPEC traits exemplify the intestinal B2 strains from Western populations.IMPORTANCE The intestinal microbiota is an important reservoir for bacteria that cause extraintestinal infections. Escherichia coli is found ubiquitously in the gut microbiota, and it also causes urinary tract infections, infantile septicemia, and meningitis. Urinary tract infections are usually caused by E. coli strains that originate in the intestinal microbiota. E. coli also causes gastrointestinal infections and is a major cause of diarrhea in infants worldwide. The abilities of certain E. coli strains to cause infections are attributed to their virulence factors, i.e., bacterial components that contribute to the development of different diseases. Our study shows that different subtypes of potentially pathogenic E. coli strains dominate in the gut microbiota of infants in different geographical areas and expands our knowledge of the interplay between bacterial commensalism and pathogenicity.

Keywords: Escherichia coli long-term persistence; ExPEC; children; enteropathogenic; intestinal microflora; phylogenetic group B2; uropathogenic.

FIG 1

Virulence scores for different B2 subgroups of commensal E. coli strains. An ExPEC virulence score was calculated by summing the virulence genes and PAIs listed in Table 2. The mean virulence score (±SD) was calculated for each B2 subgroup. Virulence scores were compared between each subgroup and all other subgroups using the Mann-Whitney U test. (a) Virulence scores for the Swedish strains. “Other” denotes strains that do not belong to any of the main B2 subgroups (subgroups I to X), i.e., STc80 (n = 6), STc567 (n = 2), and unknown STs (n = 3). “EPEC” represents EPEC lineages. (b) Virulence scores for Pakistani strains belonging to the main B2 subgroups (subgroup II = 1 strain, subgroup III = 2 strains, subgroup VI = 1 strain, subgroup VII = 2 strains, subgroup VIII = 2 strains, and subgroup IX = 1 strain) and EPEC strains (n = 9); one strain of an unknown subgroup was excluded from the analysis. As the virulence marker usp was not screened, it is not included in the virulence score for the Pakistani strains. ***, P = 0.0001 for the Swedish strains; **, P = 0.004 for the Pakistani strains.

FIG 2

Time of first appearance of different E. coli B2 subgroups in the infants’ microbiota. The E. coli B2 strains that colonized the guts of 87 Swedish infants during the first 12 months of life were subgrouped. The timing of their first appearance in the microbiota, i.e., at 0 to 2, 6, or 12 months of age, was noted. The data shown are the percentages of all B2 strains established at 0 to 2 months, 6 months, and 12 months of age. The numbers of strains belonging to each B2 subgroup at the different time points are indicated above the bars.

FIG 3

Durations of persistence in the infant microbiota of E. coli strains of different B2 subgroups. Eighty-seven infants who were followed to at least 12 months of age were colonized with 120 E. coli B2 phylogroup strains in the first year of life. For 64 of these strains, persistence in the gut could be determined. The durations of persistence of the remaining strains could not be determined, as they appeared only once at 2, 6, or 12 months of life when there were intervals of several months between the sampling occasions. The duration of persistence (days) for each strain is indicated by a symbol, and the mean value for that B2 subgroup is indicated by a bar. Strains that belonged to one of the main B2 subgroups were compared with other strains (Mann-Whitney U test). “Other” refers to strains that neither belonged to any of the 10 main B2 subgroups nor belonged to the EPEC lineages; these included strains of STc80, STc567, and single STs.