Ecogenomics and functional biogeography of the Roseobacter group in the global oceans based on 653 MAGs and SAGs

The Roseobacter group is a major component of prokaryotic communities in the global oceans. Information on this group is based predominantly on isolates and their genomic features and on the 16S rRNA gene. Assessments of prokaryotic communities in the pelagic of the global oceans indicated an unveiled diversity of this group but studies of the diversity and global biogeography of the entire group are still missing. Hence, we aimed at a comprehensive assessment of the Roseobacter group in the global oceans on the basis of MAGs and SAGs. The obtained 610 MAGs and 43 SAGs of high quality were subjected to in-depth analyses of their phylogeny, genomic and functional features. The recruitment locations range from the tropics to polar regions, include all major ocean basins. The phylogenetic analysis delineated the known RCA cluster and five pelagic clusters, two of which were completely novel: TCR (Temperate and Cold Roseobacter), AAPR (Arctic-Atlantic-Pacific Roseobacter, novel), AAR (Arctic-Atlantic Roseobacter, novel), COR (Central Oceanic Roseobacter), LUX (Cand. Luxescamonaceae) cluster. These clusters account for ~70% of all Roseobacter MAGs and SAGs in the epipelagic. The TCR, AAPR, AAR and LUX clusters are among the most deeply branching lineages of the Roseobacter group. These clusters and several sublineages of the RCA and COR clusters exhibit distinct features of genome streamlining, i.e. genome sizes of <2.9 Mbp and G+C contents of <40%. The clusters exhibit differences in their functional features and also compared to other lineages of the Roseobacter group. Proteorhodopsin is encoded in most species of the AAPR, AAR, TCR and RCA clusters and in a few species of the COR cluster, whereas in most species of the latter, the LUX cluster and in a few species of the RCA cluster aerobic anoxygenic photosynthesis was encoded. Biogeographic assessments showed that the AAPR, AAR, TCR and RCA clusters constitute the Roseobacter group in the temperate to polar regions to great extent whereas the COR and LUX clusters in the tropics and subtropics. Our comprehensive analyses shed new light on the diversification, genomic features, environmental adaptation, and global biogeography of a major lineage of pelagic bacteria.