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The reported increase in antibiotic-resistant bacteria in humans has resulted in a major shift away from antibiotic use in food animal production. This shift has been driven by the assumption that removing antibiotics will select for antibiotic susceptible bacterial taxa, which in turn will allow the currently available antibiotic arsenal to be more effective.

Salmonella enterica serovar Heidelberg (SH) is one of the prolific serovars causing poultry-associated food-borne illness in the world. Their ability to cause invasive infections and their promiscuity to plasmids that confer multidrug resistance to antibiotics of human health importance makes them a public health threat. Although, horizontal gene transfer (HGT) is recognized as the major mechanism used by Salmonella for acquiring antimicrobial resistance (AR) and virulence genes, the biology behind acquisition of new genes in SH is still unknown. In this study, we show that one day old broiler chicks challenged orally or via the cloaca with an antibiotic susceptible SH strain and raised without antibiotics carried susceptible and multidrug resistance SH strains 14 days after challenge. SH infection perturbed the bacterial community of broiler chicks and orally challenged chicks acquired AR at a higher rate than chicks challenged through the cloaca. Furthermore, SH strains lost and gained new genes, while some inverted their chromosome after colonizing the gut of broiler chicks. The acquisition of IncI1 plasmid multilocus sequence type 26 (pST26) from commensal Escherichia coli population present in the gut of broiler chicks conferred multidrug resistance phenotype to SH recipients and carriage of pST26 increased the fitness of SH under acidic selection pressure. Our results suggest that HGT shapes the evolution of AR in SH and that antibiotic use reduction alone is insufficient to limit AR plasmid transfer from commensal bacteria to Salmonella.

Antimicrobial resistance spread is a worldwide health challenge, stemming in large part from the ability of microorganisms to share their genetic material through horizontal gene transfer. To address this issue, many countries and international organizations have adopted a One Health approach to curtail the proliferation of antimicrobial-resistant bacteria.

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