Escherichia coli is a commensal species of the lower intestine, but also a major pathogen causing intestinal and extra-intestinal infections. Most studies on genomic evolution of that species focused on antibiotic resistance, using isolates sampled from infections, and neglected the evolution of virulence. Here instead, we whole-genome sequenced a collection of 436 E. coli isolated from fecal samples of healthy adult volunteers in France between 1980 and 2010. Those 436 isolates showed a high diversity. They were distributed among 159 sequence types (STs), the five most frequent being ST10 (15.6%), ST73 (5.5%) and ST95 (4.8%), ST69 (3.7%) and ST59 (3.7%) and 230 O:H serotypes. An increase in ST and serotype diversity was observed overtime. The O1, O2, O6 and O25-groups used in bioconjugate O-antigen vaccine were found in only 63% of the four main STs associated to a high risk to cause an extra-intestinal infection (ST69, ST73, ST95 and ST131). The very low risk of infection associated ST10 decreased whereas STs associated with extra-intestinal infections increased concomitantly in frequency. In the meantime, both extra-intestinal virulence-associated genes and resistance to antibiotics increased. While the evolution of resistance was dominated by an increase in resistance gene frequency within multiple STs, virulence genes evolved through both clonal expansion of STs carrying them and increases in frequency within STs. This study provides a unique picture of the phylogenomic evolution of E. coli in its human commensal habitat over a 30-year period, and has implications for O-antigen based vaccine strategy against E. coli extra-intestinal diseases.
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