Population Structure and Antimicrobial Resistance Gene Transfer of Respiratory Escherichia coli Isolated from Swine in China

Abstract Porcine respiratory diseases caused by extraintestinal pathogenic Escherichia coli (ExPEC) pose a severe threat to swine production and public health; however, research on respiratory tract-isolated ExPEC remains limited. This study comprehensively analyzed the genomic characteristics and antibiotic resistance gene (ARG) transfer potential of 442 ExPEC strains isolated from porcine lungs across 21 Chinese provinces (including 54 newly isolated strains from 2022–2024 and 388 NCBI-deposited strains). Phylogenetic analysis revealed that 84% of the isolates belonged to phylogroups A, B1, and C, with ST410, ST101, and ST88 as the predominant STs. The strains exhibited extensive ARG diversity, harboring 111 distinct ARGs, with sul2 (81.2%), floR (73.3%), and tet (A) (67.9%) being the most prevalent. Importantly, critical ARGs (e.g., bla NDM−1/5 , the mcr family, and tet (X4) ) were also detected. Notably, of the 5,818 ARG copies detected across the 442 genomes, 77.2% (4,491) were predicted to have horizontal transfer potential (co-localization with mobile genetic elements), with plasmids (especially IncF family replicons) serving as the core vectors, followed by integrons and transposons. Network analysis of ARG co-occurrence further identified aph(3'')-Ib , aph(6)-Id , sul2 , and floR as a tightly connected core module associated with the spread of multidrug resistance. Pangenomic analysis confirmed an open genome architecture, with core genes accounting for only 6%, reflecting the strains’ capacity to acquire exogenous genetic material via horizontal transfer. Moreover, the frequent joint carriage of ARGs and plasmid replicons within the same strain implies a risk of co-selective dissemination. From the One Health perspective, these transferable ARGs can spread to the environment and humans through fecal discharge and the food chain. Overall, our results highlight that ExPEC strains from porcine lungs act as important reservoirs of ARGs, pose potential risks to human health, and may even serve as sources of pathogenic agents underlying human infections, reinforcing the need for continued surveillance and control of ExPEC in swine production.