Long‐term evolution of the natural isolate of Escherichia coli 536 in the mouse gut colonized after maternal transmission reveals convergence in the constitutive expression of the lactose operon

Abstract

In vitro experimental evolution has taught us many lessons on the molecular bases of adaptation. To move towards more natural settings, evolution in the mice gut has been successfully performed. Yet, these experiments suffered from the use of laboratory strains as well as the use of axenic or streptomycin‐treated mice to maintain the inoculated strains. To circumvent these limitations, we conducted a one‐year experimental evolution in vivo using a natural isolate of E. coli, strain 536, in conditions mimicking as much as possible natural environment with mother‐to‐offspring microbiota transmission. Mice were then distributed in 24 independent cages and separated into two different diets: a regular one (chow diet, CD) and high‐fat and high‐sugar one (Western Diet, WD). Genome sequences revealed an early and rapid selection during the breastfeeding period that selected the constitutive expression of the well‐characterized lactose operon. E. coli was lost significantly more in CD than WD; however, we could not detect any genomic signature of selection, nor any diet specificities during the later part of the experiments. The apparently neutral evolution presumably due to low population size maintained nevertheless at high frequency the early selected mutations affecting lactose regulation. The rapid loss of lactose operon regulation challenges the idea that plastic gene expression is both optimal and stable in the wild.

The Selective Advantage of the lac Operon for Escherichia coli Is Conditional on Diet and Microbiota Composition

“…The emergence of constitutive mutants for lactose consumption during the first days of life was observed in a controlled experiment (Ghalayini et al, 2019), further supporting the hypothesis that the lac operon is under strong selection during this period, which in the long term could help E. coli to secure a place in the complex adult microbiota.…”

The population genomics of increased virulence and antibiotic resistance in human commensal Escherichia coli over 30 years in France

“…Whether bacteria carrying some virulence genes are better adapted to nutrient-dense diets could be experimentally tested (O’Brien and Gordon 2011). In an effort to do so, we recently analyzed how mice diet affected the density of E. coli in the mice gut and found that the B2 strains used was more prevalent in a high sugar high fat diet than in a high fiber diet (Ghalayini et al 2019). In addition to nutriment availability, protection again host immune defense, phages and protozoans also drives the evolution of virulence (Denamur et al 2021; Wildschutte et al 2004).…”

Dynamics of extended-spectrum beta-lactamase-producing Enterobacterales colonization in long-term carriers following travel abroad

“…To compute the ratio of synonymous to non-synonymous mutation rates, we counted the number of synonymous sites (S) and non-synonymous sites (N) in two diverged genomes of E. coli : strain 536 (B2 phylogroup) and REL606 (A phylogroup) [24]. We computed the rates as the total number of mutations observed (s for the synonymous, n for the nonsynonymous) divided by the number of possible sites, and the ratio of rates was computed as normalR = normaln / normalN normals / normalS .…”