Intestinal carriage of extended spectrum β-lactamase (ESBL)-producing
Escherichia coli
is a frequent, increasing and worrying phenomenon, but little is known about the molecular scenario and the evolutionary forces at play. We screened 45 veal calves, known to have high prevalence of carriage, for ESBL-producing
E. coli
on 514 rectal swabs (one randomly selected colony per sample) collected over six months. We characterized the bacterial clones and plasmids carrying
bla
ESBL
genes with a combination of genotyping methods, whole genome sequencing and conjugation assays. One hundred and seventy-three ESBL-producing
E. coli
isolates [
bla
CTX-M-1
(64.7%),
bla
CTX-M -14
(33.5%) or
bla
CTX-M-15
(1.8%)] were detected, belonging to 32 bacterial clones, mostly of phylogroup A. Calves were colonized successively by different clones with a trend in decreasing carriage. The persistence of a clone in a farm was significantly associated with the number of calves colonized. Despite a high diversity of
E. coli
clones and
bla
CTX-M
-carrying plasmids, few
bla
CTX-M
gene/plasmid/chromosomal background combinations dominated, due to (i) efficient colonization of bacterial clones and/or (ii) successful plasmid spread in various bacterial clones. The scenario ‘clone vs. plasmid spread’ depended on the farm. Thus, epistatic interactions between resistance genes, plasmids and bacterial clones contribute to optimize fitness in specific environments.
Importance
The gut microbiota is the epicenter of the emergence of resistance. Considerable amount of knowledge on the molecular mechanisms of resistance has been accumulated but the ecological and evolutionary forces at play in nature are less studied. In this context, we performed a field work on temporal intestinal carriage of extended spectrum β-lactamase (ESBL)-producing
Escherichia coli
in veal farms. Veal calves are animals with one of the highest levels of ESBL producing
E. coli
fecal carriage, due to early high antibiotic exposure. We were able to show that calves were colonized successively by different ESBL-producing
E. coli
clones, and that two main scenarios were at play in the spread of
bla
CTX-M
genes among calves: efficient colonization of several calves by a few bacterial clones and successful plasmid spread in various bacterial clones. Such knowledge should help develop new strategies to fight the emergence of antibiotic-resistance.
PixR, a Novel Activator of Conjugative Transfer of IncX4 Resistance Plasmids, Mitigates the Fitness Cost of
mcr-1
Carriage in Escherichia coli
