First report from supermarket chicken meat and genomic characterization of colistin resistance mediated by mcr-1.1 in ESBL-producing, multidrug-resistant Salmonella Minnesota

Abstract

Plasmid-borne colistin resistance is considered one of the most complex public health concerns worldwide. Several studies reported the presence of the mcr-1.1 harboring Salmonella from the foodstuffs worldwide; still, there is a knowledge gap about the occurrence of these isolates in the Middle East. In this study, we report an mcr-1.1-mediated colistin resistance in two multidrug-resistant (MDR) S. Minnesota (denoted as Sal_2 and Sal_10), with both being also extended-spectrum β-lactamase (ESBL) producing. These isolates have been recovered from two independent samples out of 315 chilled chicken meat tested from retail supermarkets in the United Arab Emirates (UAE). Based on whole-genome sequencing (WGS) analysis, both isolates belonged to the same Sequence Type (ST) ST548. They shared the same genes encoding resistance to the following antimicrobials: polymyxin (mcr-1.1), phenicol (floR), quinolone (qnrB19), aminoglycoside (aac(6')-Iaa), tetracycline (tet(A)), and sulfonamide (sul2). However, the isolates featured different patterns of β-lactamase resistance genes, which included bla_CTX-M-55 (ESBL-β-lactamase) and bla_CMY-2 (AmpC-β-lactamase) in the isolate Sal_2, and bla_TEM-215 (ESBL-β-lactamase) in the isolate Sal_10. WGS analysis inferred that both S. Minnesota isolates in this study carry an IncX4 plasmid harboring the mcr-1.1 variant. To understand the possible origin of the two mcr-1.1 carrying S. Minnesota isolated from retail chicken meat in this study, we conducted a phylogenomic analysis using available genomes of S. enterica, which harbored mcr-1.1 gene (n = 240, from the Middle East and Asian countries) deposited in the NCBI database. We found that Sal_2 and Sal_10 independently clustered together with other isolates detected in China, mainly from the chicken origin and to a lesser extent from human clinical origin. The finding of mcr-producing colistin-resistant strains in retail chicken meat warrants a more comprehensive One Health investigations involving strains from animals, retail food chains, and human clinical isolates at the national level in the UAE.

Keywords: Antimicrobial resistance; Colistin; IncX4; MCR; Poultry; Salmonella; UAE.