Evidence of ESBL plasmid transfer and selective persistence of multiple host-associated Escherichia coli isolates in a chicken cecal fermentation model

Abstract

The guts of animals and humans harbor diverse microbial communities that are regularly exposed to bacteria originating from food, water, and their surroundings. Species such as Escherichia coli are adept at colonizing multiple hosts, along with surviving in the environment. By encoding pathogenic traits and transmissible forms of antimicrobial resistance (AMR), E. coli can also pose a zoonotic risk. Our understanding of the factors that govern host residency is limited. Here, we used a chicken cecal fermentation model to study survival and the AMR transfer potential of 17 host-associated extended-spectrum β-lactamase (ESBL)-producing E. coli isolates. Vessels containing chicken cecal contents were stabilized for 4 days before the addition of a cocktail comprising ESBL-producing E. coli obtained from human, cattle, pig, and chicken hosts. Consecutive sampling showed that pig and cattle-associated isolates persisted in most vessels, although the recovery of all isolates declined over time. Increasing the inoculum dose or adding ceftiofur helped to stabilize populations of ESBL E. coli within the vessels, although this did not result in outgrowth of resistant populations in all vessels. Sequencing revealed that most new ESBL-producing E. coli recovered during the study acquired a blaCTX-M-1 plasmid from a single ESBL E. coli included in the cocktail that lacked host-specific traits (generalist). Our data highlight that isolate-specific differences in the E. coli genome composition likely explain the persistence of specific clones and efficiency of plasmid transfer, both of which could impact the spread of AMR in complex communities.IMPORTANCEThere are few insights into how host-associated Escherichia coli behave within the gut environment of other hosts. E. coli isolates that are immigrants to the gastrointestinal system of humans and animals have the potential to transfer their resistance to other native bacteria. A better understanding of this process is needed to assess how the gastrointestinal environment could serve as a reservoir and a melting pot of new, multidrug-resistant E. coli isolates