Replicon family of vibrionaceae plasmids as a reservoir of antimicrobial and phage resistance genes in marine ecosystems

Abstract

Plasmids are mobile genetic elements that drive horizontal gene transfer among bacteria, influencing microbial community composition and functional traits in marine ecosystems. However, many marine plasmids remain unclassified due to unknown replication mechanisms. Here, we describe VBR1, a novel plasmid replicon family, widespread among species of the family Vibrionaceae. The minimal VBR1 replicon comprises a 570-bp AT-rich origin of replication (oriV) and two genes, vrp1AB, sufficient for autonomous replication in Escherichia coli and Photobacterium damselae. A comprehensive GenBank search revealed 158 previously untyped plasmids from Vibrionaceae species worldwide harboring this replicon, including relevant pathogens for animals and humans as well as environmental species. VBR1 plasmids share a syntenic set of backbone genes, are predominantly conjugative, and frequently encode antimicrobial resistance (AMR) genes, conferring resistance to multiple antibiotic classes. Most VBR1 plasmids also carry phage defense and anti-defense systems, underscoring their ecological and evolutionary significance. AMR and defense/antidefense gene repertoires are highly variable across VBR1 plasmids, suggesting frequent gene acquisition, recombination events, and rapid replacement and diversification of resistance and defense determinants. The co-localization of AMR and phage defense systems on many VBR1 plasmids highlights their role in shaping virus–host interactions and microbial community dynamics. Our findings establish VBR1 as a widespread, clinically and ecologically relevant replicon family, providing a framework for the classification and surveillance of previously orphan plasmids, and advancing our understanding of AMR and phage resistance dynamics in marine ecosystems.