From ecology to evolution: plasmid- and colicin-mediated persistence of antibiotic resistant Escherichia coli in gulls

Abstract

Antimicrobial resistance in wildlife is an emerging concern within the One Health concept. Gulls, due to their synanthropic behaviour and long-distance migration, are recognised as vectors and secondary reservoirs of resistant bacteria. These birds can facilitate the environmental spread of resistant strains across ecosystem boundaries. Understanding their role in shaping microbial communities is essential for assessing the broader ecological impact. This study investigates the persistence and competitive dynamics of cephalosporin-resistant Escherichia coli in Caspian gulls captured at their breeding colony at a water reservoir and subsequently monitored in captivity for three months, representing the longest in vivo experiment of its kind conducted on wild birds. We observed sustained colonization and long-term shedding of resistant E. coli throughout the entire study, marking the longest documented carriage of resistant bacteria in wild birds to date. Notably, rapid dissemination of various E. coli sequence types (STs) with CTX-M-1 was observed, with ST11138 rapidly outcompeting other strains, including the initially dominant ST11893. Genomic analyses revealed that ST11138 harboured F24:A-:B1 and IncI1/ST3/CTX-M-1 plasmids encoding colicins and corresponding immunity genes, likely conferring a competitive advantage. Our findings underscore the role of bacteriocin-mediated interactions in shaping microbial communities and highlight the importance of plasmid-encoded traits in the persistence of resistant strains in wildlife. Importantly, our findings underscore the ecological novelty of longitudinal in vivo tracking of AMR persistence in natural hosts and highlight the need to consider ecological and microbiome-level interactions when assessing the environmental dimension of AMR under the One Health concept. ImportanceAntimicrobial resistance in wildlife is an emerging concern within the One Health framework, with gulls recognized as important vectors and secondary reservoirs of resistant bacteria. Due to their synanthropic behaviour and long-distance migration, these birds can facilitate the spread of resistant strains across ecosystems. However, the role of wildlife in resistance dynamics remains underexplored, especially in long-term, natural settings. Our study is unique in its scope and duration, representing the longest in vivo experiment of its kind conducted on wild birds. By capturing these processes in live hosts under naturalistic conditions and across an extended period, our study provides rare and ecologically grounded insights into how antimicrobial resistance is maintained outside clinical or laboratory settings. Our findings show sustained colonization and long-term shedding of resistant E. coli, with strain ST11138 outcompeting others. Genomic analyses reveal plasmid-encoded traits, highlighting the novel ecological and evolutionary mechanisms underlying resistance maintenance in wildlife.