Whole genome phylogeny of Cyanobacteria documents a distinct evolutionary trajectory of marine picocyanobacteria

During their 2.7 Gyr long evolution cyanobacteria radiated into a large number of different lineages. To better understand the evolution of cyanobacteria we compared a whole genome phylogenetic tree using 1,047 concatenated single copy orthologues of Prochlorococcus marinus MIT9313 obtained from 93 reference prokaryotic species with traditional phylogenies inferred from 16S rRNA gene and 109 genes found in all used genomes. In contrast to the traditional phylogeny, our genome wide analysis shows a split between picocyanobacteria encompassing all marine Prochlorococcus species, marine "Synechococcus" species, and members of freshwater Cyanobium genus (altogether referred here as the "PSC" clade) and the remaining groups of extant cyanobacteria. To determine the influence of the horizontal gene transfer on the overall tree topology we removed the 374 genes identified as potentially transferred genes. A newly calculated tree utilizing the remaining 673 genes displayed the same topology as the former whole genome tree with the PSC clade as a basal group of all cyanobacteria. The picocyanobacteria also exhibited distinctly larger similarity to reference bacterias cell and genome size, carboxyzome architecture, various metabolic pathways, and chlorophyll synthesis than to the other cyanobacteria. Potentially horizontally transferred genes were found in connected chains throughout fundamental metabolic pathways suggesting that evolution of these genes was severely limited and or brought to a standstill. The environment related genes connected with metabolism of nitrogen, sulfur, and scarce seawater metals were more conserved in PSC group as they were already best tuned for its poor and stable environment. Other genes were found predominantly sequentially static as they were already accurately adapted with rare beneficial mutations. The PSC clade thus represents an isolated cyanobacterial lineage which followed a distinct evolutionary trajectory driven by its specific environment.