Emergence and Genomic Characterization of the First Reported optrA-Carrying Linezolid-Resistant Enterococci Isolated from Retail Broiler Meat in the United Arab Emirates

Abstract

The foodborne transfer of resistant genes from enterococci to humans and their tolerance to several commonly used antimicrobials are of growing concern worldwide. Linezolid is a last-line drug for managing complicated illnesses resulting from multidrug-resistant Gram-positive bacteria. The optrA gene has been reported in enterococci as one of the acquired linezolid resistance mechanisms. The present study uses whole-genome sequencing analysis to characterize the first reported isolates of linezolid-resistant E. faecium (n = 6) and E. faecalis (n = 10) harboring the optrA gene isolated from samples of supermarket broiler meat (n = 165) in the United Arab Emirates (UAE). The sequenced genomes were used to appraise the study isolates’ genetic relatedness, antimicrobial resistance determinants, and virulence traits. All 16 isolates carrying the optrA gene demonstrated multidrug-resistance profiles. Genome-based relatedness classified the isolates into five clusters that were independent of the isolate sources. The most frequently known genotype among the isolates was the sequence type ST476 among E. faecalis (50% (5/10)). The study isolates revealed five novel sequence types. Antimicrobial resistance genes (ranging from 5 to 13) were found among all isolates that conferred resistance against 6 to 11 different classes of antimicrobials. Sixteen different virulence genes were found distributed across the optrA-carrying E. faecalis isolates. The virulence genes in E. faecalis included genes encoding invasion, cell adhesion, sex pheromones, aggregation, toxins production, the formation of biofilms, immunity, antiphagocytic activity, proteases, and the production of cytolysin. This study presented the first description and in-depth genomic characterization of the optrA-gene-carrying linezolid-resistant enterococci from retail broiler meat in the UAE and the Middle East. Our results call for further monitoring of the emergence of linezolid resistance at the retail and farm levels. These findings elaborate on the importance of adopting a One Health surveillance approach involving enterococci as a prospective bacterial indicator for antimicrobial resistance spread at the human–food interface.

Enterococcus species: insights into antimicrobial resistance and whole-genome features of isolates recovered from livestock and raw meat in Ghana

“…among livestock across different geographic regions can be attributed to differences in dietary patterns, which impact the composition of gut commensal bacteria ( Klibi et al, 2013 ; Ngbede et al, 2017 ). Similar to our findings, other studies ( Golob et al, 2019 ; Habib et al, 2022 ) have also reported consistent contamination of retail meat by Enterococcus spp. and this has been linked to fecal contamination.…”

Antibiotic Resistance among Gastrointestinal Bacteria in Broilers: A Review Focused on Enterococcus spp. and Escherichia coli

“…Linezolid, the first clinically available oxazolidinone, is globally used in human medicine as a last-resort antimicrobial agent to treat infections caused by multidrug-resistant Gram-positive pathogens, such as VRE [ 107 , 108 ]. This drug class is not approved for food animals in the USA and EU and, as expected, Tyson et al (2018) reported very low levels of linezolid-resistant Enterococcus spp.…”

“…(LRE) from food animal cecal content in the USA, and De Jong et al (2019) revealed that commensal enterococci from healthy cattle, pigs, and chickens across Europe and broiler breeder farms in Korea were rarely resistant to linezolid [ 69 , 93 , 109 ]. In the United Arab Emirates, Habib et al (2022) reported as well low levels of LRE from retail broiler meat [ 107 ]. Besides linezolid, daptomycin, which is a cyclic lipopeptide antibiotic, is also used for the treatment of complicated infections caused by Gram-positive organisms.…”

“…Kim et al (2018) studied the molecular characteristics of 85 E. faecalis strains isolated from chicken meat samples, and ST256 was observed in over 50% of the isolates [ 130 ]. E. faecalis strains isolated from retail chicken carcasses in the Emirate of Abu Dhabi were assigned to five different sequence types, and half of them belonged to the clonal lineage ST476 [ 107 ]. ST314, followed by ST16, were the most prevalent clonal lineages reported among broilers across Australia [ 60 ].…”

“…Kim et al (2018) isolated one E. faecium strain from chicken meat samples that was revealed to belong to ST451 [ 130 ]. E. faecium isolated from retail chicken carcasses in Abu Dhabi Emirate has been assigned to four different sequence types: one known ST (ST195) and three novel STs (ST2236, ST2238, and ST2239) [ 107 ]. ST492, followed by ST195 and ST241, were the most prevalent clonal lineages reported among broilers across Australia [ 60 ].…”