Characterization of an Extensively Drug-Resistant Salmonella Kentucky ST198 Co-Harboring cfr, mcr-1 and tet(A) Variant from Retail Chicken Meat in Shanghai, China

The emergence of extensively drug-resistant (XDR) foodborne pathogens poses grave threats to food safety. This study characterizes the genome of an XDR <i>Salmonella</i> Kentucky isolate (Sal23C1) co-harboring <i>cfr</i>, <i>mcr-1</i> and <i>tet</i>(A) from Shanghai chicken meat in 2022, which was the only isolate co-harboring these three key resistance genes among 502 screened <i>Salmonella</i> isolates. Genomic analysis revealed that the multidrug resistance gene <i>cfr</i>, which confers resistance to phenicols, lincosamides, oxazolidinones, pleuromutilins and streptogramin A, was identified within a Tn<i>3</i>-IS<i>6</i>-<i>cfr</i>-IS<i>6</i> structure on the transferable plasmid p3Sal23C1 (32,387 bp), showing high similarity to the <i>Citrobacter braakii</i> plasmid pCE32-2 (99% coverage, 99.98% identity). Concurrently, the <i>mcr-1</i> gene resided in a <i>pap2</i>-<i>mcr-1</i> structure on the transferable IncI2 plasmid p2Sal23C1 (63,103 bp). Notably, both genes could be co-transferred to recipient bacteria via conjugative plasmids at frequencies of (1.15 ± 0.98) × 10^-6. Furthermore, a novel ~79 kb multidrug resistance region (MRR) chromosomally inserted at the <i>bcfH</i> locus was identified, carrying <i>fosA3</i>, <i>mph</i>(A), <i>rmtB</i>, <i>qnrS1</i> and <i>bla</i>_CTX-M-55. Additionally, a novel <i>Salmonella</i> Genomic Island 1 variant (SGI1-KI) harbored <i>aadA7</i>, <i>qacEΔ1</i>, <i>sul1</i> and the <i>tet</i>(A) variant. The acquisition of these antibiotic resistance genes in this isolate enhanced bacterial resistance to 21 antimicrobials, including resistance to the critical last-resort antibiotics tigecycline and colistin, which left virtually no treatment options for potential infections. Taken together, this is the first comprehensive genomic report of an XDR poultry-derived <i>Salmonella</i> Kentucky isolate co-harboring <i>cfr</i>, <i>mcr-1</i> and the <i>tet</i>(A) variant. The mobility of these resistance genes, facilitated by IS<i>6</i> elements and conjugative plasmids, underscores significant public health risks associated with such isolates in the food chain.