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Our study aimed to characterize the faecal microbiota and acquired resistome of Ross-308 roosters in Hungary. Amplicon and shotgun metagenomics revealed a faecal microbiota dominated by the Firmicutes, Bacteroidota, and Proteobacteria and a diverse faecal resistome, including qnrB and an aadA1-bearing integron. Culture-based screening of an antibiotic-free rooster yielded the MDR Escherichia coli strain K1G, displaying resistance also to third-generation cephalosporins and fluoroquinolones. Whole-genome sequencing classified K1G as a serotype O23:H16-ST453 avian pathogenic E. coli (APEC) strain featuring a set of chromosomal virulence factors (including astA, hlyE, lpfA, and iss) and three plasmids: a phage-like plasmid, a mosaic virulence plasmid (carrying blaTEM-1b, hlyF, iutA, ompT, iucD, and cvaC), and an IncC type 1 resistance plasmid harbouring blaCMY-2. The detection of identical or closely related ST453 E. coli strains also in broiler meat in Hungary highlights a potential risk of transmission to humans through the food chain. 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