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Genomic analysis reveals close genetic similarity between ESBL-producing E. coli isolates from humans and dogs, suggesting potential for inter-species transmission

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Jul 28, 2025 version files 1.62 MB

Abstract

Introduction: Extended-spectrum β-lactamase-(ESBL) producing Enterobacteriaceae are emerging in hospital and community settings as important causes of urinary tract infections. This group of plasmid-mediated enzymes has been identified primarily in human and dog hosts with blaCTX-M’s being most prevalent ESBLs worldwide. Our objective was to identify horizontal gene transfer(HGT) events amongst human and dog-derived ESBL-producing bacteria by examining genetic relatedness of plasmid and bacterial whole genome sequences(WGS) associated with ESBLs. By understanding genetic relatedness, we aimed to provide insight into transmission dynamics of ESBLs and antibiotic resistance among humans and dogs in community-acquired settings.

Methods: DNA was extracted from 16 Uropathogenic E. coli (UPEC) strains from humans to determine plasmid sequences using Nanopore Technology. Plasmid sequences acquired in Nanopore were used as references to collect ESBL-producing plasmid sequences (N = 149) and WGS (N = 109) from the National Center for Biotechnology Information (NCBI) database (accessed August 2022-July 2023). The Bacterial and Viral Bioinformatic Resource Center (BV-BRC), Comparative Antibiotic Resistance Database (CARD), plasmid Multi-Locus Sequence Typing (pMLST), Center for Genomic Epidemiology (CGE), and Multi-Locus Sequence Typing (MLST) were used to analyze plasmid and whole genome sequences. Phylogenetic analysis was also performed on plasmid and whole genome sequences.

Results: Of 149 plasmids collected from humans (n = 125) and dogs (n = 24), 110(73.8%) were class A ESBLs with blaCTX-M-14 (32%), and blaTEM-1 (32%), predominant among the human population and blaCTX-M-1 (31%) and blaTEM-1 (27%) among the dog population. pMLST showed that IncF, IncI1, and IncN plasmids were the main groups contributing to dissemination of ESBLs amongst human and dog populations. Genome annotations revealed that plasmids carrying ESBLs harbored genes responsible for HGT by conjugation. Neighbor-joining cluster analysis showed human and dog-derived plasmids do share ESBL genes and other antibiotic-resistant genes(ARGs). The maximum-likelihood tree revealed a high predominance of ST-131 carried by E. coli serotypes O25:H4 amongst humans and dogs. Virulence gene identification showed that UPEC strains were not the only carriers of ESBL-producing bacteria.

Discussion: Results revealed evidence of cross-species transmission of ESBLs between humans and dogs at plasmid and E. coli clonal levels, underscoring the need to increase surveillance of ARGs in the community to mitigate ESBL transmission in community settings.