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.

Bacterial “Virulence” Traits and Host Demographics Predict Escherichia coli Colonization Behaviors Within Households

“…Here, phylogroups B2 and D ranked highest for fecal predominance, persistence, and prevalence and second highest (after phylogroup F) for sharing. This aligns generally with evidence that phylogroup B2—the most extraintestinal pathogenic E. coli phylogroup—corresponds with within-household strain sharing [ 12 , 14 , 19 , 32 , 37 , 38 ]. Likewise, here phylogroup B1, generally regarded as less virulent, was associated negatively with fecal colonization.…”

“…Conceivably, superior colonization/sharing ability contributes to these lineages’ epidemiological success. By contrast, ST73, another prominent cause of extraintestinal E. coli infections [ 31 ] that in previous studies exhibited increased sharing and persistence [ 12 , 32 ], here was associated negatively with household prevalence. These between-study and between-lineage differences suggest that although virulence and commensalism may align generally, exceptions occur, perhaps related to specific lineages and/or host populations or stochastic factors.…”

“…Some propose that E. coli virulence genes are byproducts of commensalism, with certain traits promoting both colonization and infection-causing ability [ 6 ], as supported by human epidemiological observations and animal model studies [ 7–9 , 12–14 , 19 , 21 , 32 , 41 ]. Our work supports this paradigm of co-evolution of virulence and commensalism, expands the number of clonal lineages and virulence factors known to be associated with gut colonization, and suggests that host factors also may play an important role in E. coli household colonization dynamics.…”

Major role of iron uptake systems in the intrinsic extra-intestinal virulence of the genus Escherichia revealed by a genome-wide association study

“…The full list of the 370 strains used in the association analysis, together with their main characteristics is reported in S1 Table . These strains belong to various published collections: ECOR (N = 71) [ 31 ], IAI (n = 81) [ 14 ], NILS (N = 82) [ 33 ], Septicoli (N = 39) [ 10 ], ROAR (N = 30) [ 34 ], Guyana (N = 12) [ 32 ], Coliville (N = 8) [ 35 ], FN (N = 6) [ 36 ], COLIRED (N = 3) [ 37 ], COLIBAFI (N = 2) [ 7 ], correspond to archetypal strains (N = 7) or are miscellaneous strains from our personal collections (N = 29). The isolation host is predominantly humans (N = 291), followed by animals (N = 72) and some strains were isolated from the environment (N = 6).…”

Characterization of Antimicrobial Susceptibility, Extended-Spectrum β-Lactamase Genes and Phylogenetic Groups of Enteropathogenic <italic>Escherichia coli</italic> Isolated from Patients with Diarrhea

“…Phylogenetic analysis of E. coli clinical strains provides information about the frequency of occurrence in the environment, and based on the presence or absence of certain genes and DNA fragments (including chuA, yjaA, arpA genes and a DNA fragment TspE4.C2), E. coli can be classified into phylogenetic groups (A, B1, B2, C, D, E and F) [ 11 ]. Majority of commensal E. coli strains belong to phylogroups A and B1 [ 12 ], and extraintestinal pathogenic E. coli mainly belongs to phylogroups B2 and D [ 13 ]. However, as the arrangement of phylogroups for diarrheagenic E. coli is still unclear, EPEC could belong to any of the phylogroups [ 14 , 15 ].…”