Ocean's twelve: Flagellar and biofilm chromids in the multipartite genome of Marinovum algicola DG898 exemplify functional compartmentalization

Summary The marine bacterium Marinovum algicola DG898 is a representative of the Roseobacter group (Rhodobacteraceae, Alphaproteobacteria) and harbours a wealth of 11 extrachromosomal replicons (ECRs) unprecedented for Proteobacteria. The relevance of ECRs has previously been exemplified by photosynthesis and biofilm plasmids, but the evolutionary forces for the emergence of multipartite genomes are largely unknown. The newly established genome revealed the exceptional metabolic potential of Marinovum and its adaptation to the phycosphere. Comparative codon usage analyses allowed the identification of eight chromids and three plasmids. Functional gene clustering is documented by the 52-kb biofilm chromid that is required for surface attachment. The most conspicuous finding is the presence of a highly expressed chromid-encoded flagellum gene cluster (FGC, fla2) that is indispensable for swimming motility. Marinovum algicola DG898 harbours an additional chromosome-encoded flagellum (fla1) with unknown function. Comprehensive phylogenetic analyses revealed the presence of a third FGC type (fla3) in Rhodobacteraceae and indicated the transmission of complete FGCs via conjugation. The current Marinovum study indicates a functional correlation of the intracellular fla2-chromid localization and the subcellular positioning of the flagellum. The proposed mechanism might represent – apart from horizontal transfer – a novel driving force for the emergence of multipartite genomes.