Abstract
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.
Abstract Importance Consumer preference for raised without antibiotics chicken meat has led to a significant reduction in antibiotics used in poultry production. However, the notion that chickens raised antibiotic-free carry reduced antibiotic resistance bacteria remains an open question. This research demonstrates that a susceptible Salmonella enterica can acquire antimicrobial resistance from commensal bacteria, even without the presence of antibiotic specific selective pressure in an antibiotic free environment. We demonstrate that selective pressure due to acidic pH is driving the recombination of genetic material including antimicrobial resistance genes and indicates that simply removing antibiotics from the environment might not be sufficient to limit the prevalence of antimicrobial resistance in broiler chicken production. These conclusions are impactful and of broader interest to the areas of food safety, agricultural production, human and animal health and add an important perspective to the ongoing debate regarding alleviating antibiotic and antimicrobial impact on the future of human health.