On the trail of oxygenic photosynthesis in deep-branching Cyanobacteria on early Earth.

The geological record offers evidence of phototrophic mats / stromatolites dating back to at least 3.2 Ga. Oxygenation of the atmosphere on early Earth during the Great Oxygenation Event (GOE), ca 2.4 Ga, is attributed to cyanobacterial growth and the contemporaneous decline of reducing volcanic gasses and oceanic hydrothermal circulation. While oxygenic photosynthesis is well studied in the modern-day oceans, extraordinarily little is known as to how early Cyanobacteria responded to the anoxic and iron-rich Archean marine environment with respect to homeostasis, growth, iron uptake and mineral formation. In this Habilitation, I present data generated under simulated Archean conditions using deep branching species that provides insight into cyanobacterial growth during the Archean. Iron is essential for photosynthesis, however, it was hypothesised that the high availability of Fe(II) on early Earth may have been toxic for early Cyanobacteria by encasing them in rust and inducing oxidative stress. Our results demonstrate that early Cyanobacteria species that are actively photosynthesising are not encrusted by rust under Archean ocean Fe(II) concentrations. Reduced growth rates under repeated Fe(II) exposure are offset against increased photosynthetic activity when compared to modern oxygen-rich conditions. The genetic potential of these deep branching stem Cyanobacteria with respect to iron acquisition suggests a role for ligand bound iron uptake. We present evidence that the early branching Pseudanabaena sp. PCC7367 grows faster and upregulates superoxide dismutase activity under simulated Archean conditions. Nitrogen fixation would have enabled Cyanobacteria to colonise N-deficient aquatic and terrestrial environments. We investigated the potential effects of changing pO2 and pCO2 on the δ15N fractionation signal and found it to be stable for MoFe nitrogenase under all atmospheres tested. In addition, we tracked this signal across an ancient volcanic basin, as well as stromatolites, revealing novel aspects of N cycling during the Archean. Overall, the data presented in this Habilitation provides a more detailed insight into the cyanobacterial primary productivity, allowing elucidation of the process of oxygenation of the Earth's hydrosphere and atmosphere in the run-up to the GOE.