The discovery of multidrug resistant Staphylococcus aureus harboring novel SaRI isolated from retail foods

Abstract

Food-borne Staphylococcus aureus has shown multidrug resistance. According to our previous studies, most S. aureus isolated from retail foods in China exhibited resistance to a variety of antimicrobials. Further Genome Wide Association Study (GWAS) revealed that a novel gene cluster, containing erythromycin-resistant genes, mef (D)- msr (F), existed in 19 isolates. In this study, we aim to investigate the distribution and transmission of this novel gene cluster in these isolates and to further characterize it. As a result, the msr (F)-positive S. aureus isolates mainly belong to ST7 (n = 14), sporadically to ST14 (n = 4), and ST88 (n = 1) most of which showed multidrug resistance (MDR) phenotype. Different virulence factors (VFs) and antimicrobial resistance genes (ARGs) were identified by genomic mining in msr (F)-positive strains. In addition, core genome phylogenetic analysis revealed that most of the msr (F)-positive strains (14/19) were closely related despite different isolation time. Two types of antibiotic resistance islands, SaRI msr -I (15.1 kb) and SaRI msr -II (16–17 kb) carrying mef (D)- msr (F), were identified in their chromosomes. Importantly, the novel SaRI msr -I was inserted into rpsI gene which encoded 30S ribosomal protein S9 on the chromosome. SaRI msr -II was also inserted into rpsI but four ORF frames downstream of rpsI were absent. Within the SaRI msr -I and -II, an operon structure consisting of ARGs, mef (D) and msr (F), and a site-specific integrase gene int were identified. Finally, the excision and cyclization of the SaRI msr and operon mef (D)- msr (F) were verified by two-step PCR. This study is the first report of MDR S. aureus harboring novel SaRI msr isolated from retail foods, indicating that this novel SaRI msr harboring mef (D)- msr (F) is distributed in food-related S. aureus in China and is one of the determinants for erythromycin resistance. The occurrence and propagation of similar mef (D)- msr (F)-carrying SaRI msr from S. aureus need further investigation. • SaRI msr carrying mef (D)- msr (F) operon emerged in MDR S. aureus for the first time. • SaRI msr was novel structure, and both SaRI msr and mef (D)- msr (F) operon were active. • The novel SaRI msr were discovered via Genome Wide Association Study (GWAS). • This novel SaRI msr harbouring mef (D)- msr (F) in DMR S. aureus should be underscored.