TIMING OF CYANOBACTERIAL ADAPTATIONS FROM FRESHWATER TO MARINE ECOSYSTEMS – A POSSIBLE KEY TO UNDERSTANDING THE RISE IN ATMOSPHERIC OXYGEN

Cyanobacteria have profoundly affected oceanic and atmospheric chemistry, culminating in the rapid oxygenation of the atmosphere by 2.32 Giga-annum before present (Ga). Carbon isotopic fractionation and lipid biomarkers suggest Cyanobacteria originated by 3.5 and 2.7 Ga. However unambiguous cyanobacterial microfossils with cell diameters >3.5 µm are not observed until ~2.0 Ga, long after the rise in oxygen. When the Cyanobacteria originated and diversified, and what their ancient traits were, remain critically unresolved problems. Here, ancestral character state reconstructions and relaxed molecular clocks were used to show that the early Cyanobacteria were restricted to low salinity, freshwater environments until about 2.4 Ga. At this time, the Cyanobacteria underwent a rapid series of diversifications, and began to colonize brackish and marine environments. On the Earth today, surface freshwater accounts to about 1 x 10^5 km^3 in lakes (87%), swamps (11%), and rivers (<1%). In comparison, the volume of the oceanic photic zone is roughly twice that, or about 2 x 10^5 km^3. This expansion in niche space would have contributed to higher fluxes of oxygen, as would have the increased availability of nutrients at continental margins and abundant concentrations of iron in the early Paleoproterozoic oceans. However, the notable difference would have been with respect to the fate of organic carbon. Once Cyanobacteria colonized marine ecosystems, organic carbon could be sedimented into the deep oceans and subducted, allowing oxygen to accumulate in the near surface and atmosphere. The rapid diversification of brackish and marine cyanobacterial lineages at 2.4 Ga could provide the explanation as to why atmospheric oxygen rose so rapidly on the early Earth. It could also explain two curious observations in the rock record between 2.3-2.2 Ga: the deposition of large amounts of organic carbon, and a global carbon isotopic excursion in marine carbonates sometimes referred to as the "Lomagundi Event". Over the next several hundred million years, marine and freshwater Cyanobacteria acquired many of the traits that we are familiar with today: large cell diameters (>3.5 µM), filamentous growth, nitrogen fixation, and the ability to form dense microbial mats.