Think pink: photosynthesis, plasmids and the Roseobacter clade

Aerobic anoxygenic photosynthesis providing additional ATP for a photoheterotrophic lifestyle is characteristic for several representatives of the marine Roseobacter clade. The patchy distribution of photosynthesis gene clusters (PGCs) within this lineage probably results from horizontal transfers and this explanation is supported by two cases of plasmid-located PGCs. In this study sequencing of the three Sulfitobacter guttiformis plasmids (pSG4, pSG53, pSG118) was initiated with the objective to analyse the 118 kb-sized photosynthetic replicon, but our annotation revealed several additional important traits including key genes of the primary metabolism. The comparison of the two photosynthesis plasmids from S. guttiformis and Roseobacter litoralis showed that their replication modules are located at precisely the same position within the 45 kb-sized PGC. However, comprehensive phylogenetic analyses of the non-homologous replicases (RepB-III, DnaA-like I) and the two ParAB partitioning proteins unequivocally document an independent origin of their extrachromosomal replicons. The analogous positioning within the two photosynthesis super-operons can be explained by a two-step recombination scenario and seems to be the ultimate result of stabilizing selection. Our exemplary analyses of 'pink' plasmids document that chromosomal outsourcing is a common phenomenon in the Roseobacter clade and subsequent horizontal exchanges offer rapid access to the marine pan-genome.