Lessons from twenty years of the life of commensal Escherichia coli populations in a human gut

Escherichia coli is an increasingly antibiotic-resistant opportunistic pathogen. Few data are available on its ecological and evolutionary dynamics in its primary niche, the vertebrate gut. Using Illumina and/or Nanopore technologies, we sequenced whole genomes of 210 E. coli natural isolates from 22 stools sampled during a 20-year period in a healthy man (ED) living in France, who did not take any antibiotics. All the phylogroups, except the C, were represented with a predominance of B2 (34.3%), followed by A and F (19% each) phylogroups. Thirty five clones were identified and classified in three phenotypes according to their abundance and persistence time: 25 sub-dominant/transient (52 isolates), five dominant/transient (48 isolates) and five dominant/resident (110 isolates). Four out of the five dominant/resident clones belonged to B2 phylogroup [sequence types (STs)131 and 452] and F-ST59, whereas sub-dominant/transient clones belonged mainly to numerous distinct B1, A and D phylogroup STs. The long residence time of B2 phylogroup clones was counterbalanced by lower colonization ability. Residence time and within-host frequency were positively correlated. By comparing ED strain genomes to a collection of commensal E. coli genomes from 359 French individuals, enriched/specific ED strain genome traits were identified including a metabolic pathway ( mhp cluster) and a very rarely reported antiviral defense island encompassing dGTPase and/or Detocs systems. SNP analysis of clonal diversity showed neutral evolution. The normal E. coli gut microbiota is shaped by both the intrinsic properties of the strain lineages and the environmental constraints.