Horizontal gene transfer is the main driver of antimicrobial resistance in broiler chicks infected with Salmonella enterica serovar Heidelberg

Overuse and misuse of antibiotics in clinical settings and in food
production have been linked to the increased prevalence and spread of
antimicrobial resistance (AR). Consequently, public health and consumer
concerns have resulted in a remarkable reduction in antibiotics used for
food animal production. However, there are no data on the effectiveness of
antibiotic removal in reducing AR shared through horizontal gene transfer
(HGT). In this study, we used neonatal broiler chicks and Salmonella
enterica serovar Heidelberg (SH), a model food pathogen, to test if chicks
raised antibiotic-free harbor transferable AR. We challenged chicks with
an antibiotic susceptible SH strain using various routes of inoculation
and determined if SH isolates recovered carried plasmids conferring AR. We
used antimicrobial susceptibility testing and whole genome sequencing
(WGS) to show that chicks grown without antibiotics harbored antimicrobial
resistant SH population 14 days after challenge and chicks challenged
orally acquired AR at a higher rate than chicks inoculated via the cloaca.
Using 16S rRNA gene sequencing we found that SH infection perturbed the
microbiota of broiler chicks and used metagenomics and WGS to confirm
commensal Escherichia coli population as the main reservoir of IncI1
plasmid acquired by SH. The carriage of this IncI1 plasmid posed no
fitness cost to SH but increased its fitness when exposed to acidic pH in
vitro. These results suggest that HGT of plasmids carrying AR shaped the
evolution of SH and that antibiotic use reduction alone is insufficient to
limit antibiotic resistance transfer from commensal bacteria to
Salmonella.