Genomic characterization of avian pathogenic <i>Escherichia coli</i> and its potential as a marker organism for antimicrobial resistance

ABSTRACT Avian pathogenic Escherichia coli (APEC) poses a threat to poultry and public health due to its ability to cause avian disease, potentially contribute to foodborne illness, and carry antimicrobial resistance genes (ARGs). Given its ubiquitous nature and capacity to persist in diverse environments, APEC has potential as a marker organism for tracking antimicrobial resistance (AMR) in poultry production systems and surrounding environments. This study investigated the prevalence, genotypic diversity, AMR profile, and potential transmission of APEC across different production stages in commercial, vertically integrated broiler operations. APEC isolates were recovered from environmental samples across the production chain, including pullet, breeder, and broiler farms as well as processing plants. E. coli isolates were classified as APEC if carrying three or more out of five virulence genes. Whole genome sequencing was conducted on 42 APECs. We determined their serotypes, phylogroups, sequence types (ST), and AMR profiles and constructed a single-nucleotide polymorphism (SNP)-based phylogenetic tree. High-risk APEC strains were detected, with ST131 recovered at the post-chill stage, raising food safety concerns. All isolates shared a core resistome, while several ARGs were differently distributed across sample types. SNP analysis revealed genetically closely related APEC strains inside the poultry house and the adjacent outside environment, and critically, between broiler litter and carcass rinses collected at the processing plant that processed the same flock. We demonstrate APEC carrying clinically relevant ARGs spread within farm environment and along the production chain, supporting its utility for AMR surveillance. IMPORTANCE Avian pathogenic Escherichia coli (APEC) is a threat to poultry production and public health due to its ability to cause avian disease, economic losses, potential foodborne implications, and ability to carry antimicrobial resistance genes (ARGs) relevant to human health. In this study, we proposed APEC as a potential marker organism of antimicrobial resistance (AMR) due to its capacity to persist in diverse environments. Our findings show that APEC, across the vertically integrated poultry production chain, harbored clinically important ARGs and exhibited resistance to antimicrobials of human health importance. We also identified evidence of APEC transmission within the farm environment and into the processing plant, with the potential to reach consumers. By examining multiple stages of production and diverse environmental samples, our study provides a more comprehensive understanding of APEC ecology, its resistome, and dissemination. These insights highlight APEC’s utility as a marker organism for AMR surveillance in poultry production.