Abstract
Plasmid-mediated antimicrobial resistance is a major contributor to the spread of resistance genes within bacterial communities. Successful plasmid spread depends upon a balance between plasmid fitness effects on the host and rates of horizontal transmission. While these key parameters are readily quantified in vitro, the influence of interactions with other microbiome members is largely unknown. Here, we investigated the influence of three genera of lactic acid bacteria (LAB) derived from the chicken gastrointestinal microbiome on the spread of an epidemic narrow-range ESBL resistance plasmid, IncI1 carrying blaCTX-M-1, in mixed cultures of isogenic Escherichia coli strains. Secreted products of LAB decreased E. coli growth rates in a genus-specific manner but did not affect plasmid transfer rates. Importantly, we quantified plasmid transfer rates by controlling for density-dependent mating opportunities. Parametrization of a mathematical model with our in vitro estimates illustrated that small fitness costs of plasmid carriage may tip the balance towards plasmid loss under growth conditions in the gastrointestinal tract. This work shows that microbial interactions can influence plasmid success and provides an experimental-theoretical framework for further study of plasmid transfer in a microbiome context.
Highlights
Plasmids are primary drivers of the spread and persistence of antimicrobial resistance genes in human and animal microbiomes [1,2,3,4]
We show that secreted products from lactic acid bacterial genera derived from the chicken gastrointestinal microbiome substantially reduce E. coli strain growth rates, while not causing reductions in conjugation rates
Using a mathematical model of continuous-flow bacterial population dynamics parametrized with our in vitro estimates, we predict that the secreted products would increase the chance of plasmid loss under conditions mimicking growth in the gastrointestinal tract
Summary
Plasmids are primary drivers of the spread and persistence of antimicrobial resistance genes in human and animal microbiomes [1,2,3,4]. Narrow-host-range IncI1 plasmids carrying the blaCTX-M-1 gene which encodes an extended-spectrum β-lactamase (ESBL) [36] are primarily detected in E. coli and Salmonella species [37]. This resistance gene–plasmid combination has been reported as the most abundant in Dutch broiler chickens [38] and in other livestock animals (including dairy cattle and slaughter pigs) in a recent 10-year surveillance study [5], despite a steady decrease in the usage of β-lactam antibiotics in The Netherlands over the past 5–10 years [39]. Using a continuous-flow mathematical model, we showed that minor changes in plasmid fitness costs could shift the balance from plasmid fixation to plasmid loss under culture conditions mimicking growth in the chicken caecum
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Free) 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
