Cross-species and cross-border spread of aph(3′)-ia -mediated neomycin resistance in Escherichia coli from animals: a genomic perspective

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BACKGROUND AND OBJECTIVES: Neomycin is widely used in livestock to control colibacillosis. Resistance among clinical Escherichia coli is increasing, likely driven by the use of this aminoglycoside following the European restrictions on zinc oxide and colistin. The aim of this study was to investigate the genetic epidemiology of neomycin-resistant E. coli across six animal species and five European countries. METHODS: A total of 750 neomycin-resistant E. coli isolates were included, combining retrospectively identified genomes with prospectively isolated and sequenced strains from multiple animal species. Genomic analyses, based on short reads (n = 529), long reads (n = 177), or hybrid assemblies (n = 44), included phylogenetic comparison, and identification of neomycin resistance genes and their genetic contexts. RESULTS: Neomycin resistance was mediated by aph(3')-Ia in 98.2% of the isolates, which were distributed across 28 clonal complexes, predominantly CC10, which was frequently detected in all countries and hosts. aph(3')-Ia was primarily carried by conjugative plasmids of diverse replicon types (70.3%) and embedded in two transposons (Tn903 and Tn4352) and three newly identified genetic elements, while a chromosomally integrated element accounted for the remaining 29.7%. Plasmids carrying aph(3')-Ia frequently co-harboured tetracycline and trimethoprim-sulfamethoxazole resistance genes, with IncX1 plasmids additionally containing chloramphenicol and quinolone resistance determinants. Phylogenetic analysis revealed dissemination of plasmid-borne elements across multiple lineages, while the chromosomal element was mostly restricted to ST117, ST88, and ST189. CONCLUSIONS: The spread of neomycin resistance in E. coli from European livestock is primarily driven by the mobility of aph(3')-Ia embedded in diverse genetic contexts and plasmid backbones, promoting co-transfer of other resistance determinants.

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