FRESHWATER TO MARINE DIVERSIFICATIONS OF THE CYANOBACTERIA AND EUKARYOTIC ALGAE – IMPLICATIONS FOR THE STEP-WISE OXYGENATION OF THE BIOSPHERE FROM THE PALEOPROTEROZOIC TO THE NEOPROTEROZOIC

A phylogenomic approach was used to resolve the branching relationships within the Cyanobacteria and eukaryotic algae, using whole genome and plastid sequences. The ancestral Cyanobacteria were inferred to have inhabited low-salinity, terrestrial environments. Separate adaptations into the marine environment were seen higher up in the tree: in the Synechococcus-Prochlorococcus (SynPro) clade, the clade containing Leptolyngbya and Plectonema (LPP), and in the clade (SPM-PNT) containing taxa with large cell diameters. Eukaryotic algal chloroplasts branched early in the cyanobacterial tree, after the node leading to the SynPro clade and before diversification of the LPP, SPM, and PNT clades. A freshwater algal ancestor was inferred, consistent with it branching early in the cyanobacterial tree before cyanobacterial colonization of the marine environment.

Next, relaxed molecular clocks were used to infer the antiquity of cyanobacterial and algal clades. Freshwater eukaryotic algae were inferred to have originated at about the time of the initial oxygenation of the Earth’s atmosphere, just prior to the diversification of marine Cyanobacteria in the SPM and PNT clades. The sudden rise in atmospheric oxygen in the Paleoproterozoic, therefore, may have been caused by early appearance of terrestrial Cyanobacteria and eukaryotic algae, followed by the initial diversification of marine Cyanobacteria. The appearance of freshwater oxygenic phototrophs would have delivered oxygen directly into the atmosphere, being spatially cut off from abundant reducing sinks in the oceans. Also, the initial diversification of marine Cyanobacteria would have increased the delivery of abundant organic carbon into deep marine sedimentary environments, further facilitating the rise in oxygen. Finally, a major diversification in marine picoplankton in the SynPro clade was inferred to have occurred in the late Neoproterozoic. This would have also increased oxygen tensions in shallow marine environments, resulting in diffusion of oxygen into the atmosphere and sedimentation of larger amounts of organic carbon into deep marine sediments. As such, the diversification of an important cyanobacterial group likely had a critical role in the origin and early evolution of animals.