Abstract
Summary Alphaproteobacteria are typically characterized by a multipartite genome organization with a chromosome, stable chromids and accessory plasmids. Extrachromosomal elements determine the lifestyle of roseobacters and their horizontal transfer was previously correlated with rapid adaptations to novel ecological niches. We characterized the distribution and biology of a novel Rhodobacteraceae ‐specific plasmid type that was designated RepC_soli according to its diagnostic solitary replicase. This low copy number replicon exhibits an exceptional stability, which is likely ensured by non‐canonical separate parA and parB partitioning genes. RepC_soli plasmids occur frequently in the surface‐associated marine genus Phaeobacter and comparative genome analyses revealed the emergence of four compatibility groups. The universal presence of conserved type IV secretion systems in RepC_soli plasmids is indicative of their recurrent mobilization, a prediction that was experimentally validated by conjugation of the 57 kb Phaeobacter inhibens P72 plasmid (pP72_e) over genus borders. RepC_soli plasmids harbour a diverse collection of beneficial genes including transporters for heavy metal detoxification, prokaryotic defence systems and a conspicuous abundance of antibiotic resistance genes. The pP72_e‐encoded efflux pump FloR conferred an about 50‐fold increase of resistance against chloramphenicol. Its specific occurrence in Phaeobacter likely reflects a genetic footprint of (former) antimicrobial use in marine aquaculture.