Emergence of Transferable <i>mcr-9</i> Gene-Carrying Colistin-Resistant <i>Salmonella enterica</i> Dessau ST14 Isolated from Retail Chicken Meat in Korea

Abstract

Colistin is an important antibiotic currently used to manage infections caused by multidrug-resistant pathogens in both humans and livestock animals. A new mobile colistin-resistance (<i>mcr-9</i>) gene was recently discovered; this discovery highlighted the need for rigorous monitoring of bacterial resistance against colistin. <i>Salmonella</i> is one of the major pathogens responsible for foodborne illnesses; however, there is minimal information regarding the presence of <i>mcr</i> genes in foodborne <i>Salmonella</i> strains. The aim of this study was to investigate the presence of <i>mcr</i> genes among 178 <i>Salmonella</i> strains isolated from chicken meat in Korea. Antimicrobial susceptibility was measured using the broth microdilution method. Bioinformatics characterization of colistin-resistant strains and genetic environment of the <i>mcr-9</i> gene were analyzed using next-generation sequencing. Transferability of the <i>mcr-9</i> carrying colistin-resistant <i>Salmonella</i> strain was tested using broth-mating conjugation. Thirteen of the 178 <i>Salmonella</i> isolates showed colistin resistance, but only one strain, <i>Salmonella</i> Dessau ST14 (KUFSE-SAL043) from a traditional chicken market in Korea, carried an <i>mcr</i> family gene, <i>mcr-9</i>. This strain also carried other acquired antimicrobial resistance genes such as <i>bla</i>_TEM-1B, <i>qnrS1</i>, and <i>aac(6')-Iaa</i>. Only the IncX1 plasmid replicon type was detected in this strain. In the strain KUFSE-SAL043, the <i>mcr-9</i> gene was located between two insertion sequences, IS<i>903B</i> and IS<i>26</i>, followed by the downstream regulatory genes <i>qseB</i>-like and <i>qseC</i>-like, which were located between IS<i>1R</i> and <i>Δ</i>IS<i>1R</i>. Conjugation tests revealed that the <i>mcr-9</i> gene was successfully transferred to <i>Escherichia coli</i> J53 at a mean frequency of 2.03 × 10^-7. This is the first report of a transferable <i>mcr-9</i> gene in <i>Salmonella</i> isolated from chicken meat in Korea, highlighting the possibility of transfer of colistin resistance. Therefore, the wide use of colistin should be reconsidered, and a One Health perspective should be adopted to monitor the antimicrobial resistance of <i>Enterobacteriaceae</i> strains in humans, livestock, and the environment.