Ecogenomics and diversification of the Roseobacter RCA cluster and global biogeography of sublineages. Metagenome-assembled genomes of the Roseobacter RCA cluster (Planktomarina)

The RCA (Roseobacter clade affiliated) cluster is a major Roseobacter lineage in temperate to polar oceans. Despite its prevalence and abundance, only a few genomes and one described species exist. To gain more insights into the genomic and functional diversity and biogeography of this cluster, we screened metagenomic datasets from the global oceans and reconstructed 82 metagenome-assembled genomes (MAG) affiliated to this cluster. These MAGs plus five genomes of isolates subdivide into three genera: Planktomarina, Pseudoplanktomarina and Paraplanktomarina. A1, the only Paraplanktomarina species, is the most deeply-branching. Its genome size of 2.40 Mbp is in the same range as that of the four Pseudoplanktomarina species but its G+C content of 45.85% is higher. Six of the eight Planktomarina species have a larger genome and the G+C content of all is higher than that of species A1. Aerobic anoxygenic photosynthesis (AAP) is encoded only in species C6 to C8 of Planktomarina. Unexpectedly, proteorhodopsin (PR) is encoded in all other Planktomarina as well as in all Pseudoplanktomarina species, indicating that this light-driven proton pump is the most important mode of acquiring complementary energy of the RCA cluster. Pseudoplanktomarina species exhibit gene content differences pointing to more streamlining relative to species A1 and adaptation to more resource-limited conditions whereas all except one Planktomarina species encode more genes. Global biogeographic patterns of the different species reflect largely their different genomic features. Our very detailed MAG-based analyses shed important light into the diversification, environmental adaptation and global biogeography of a major lineage of pelagic bacteria.