Abstract
The evolution of Photosystem II changed the history of life by oxygenating the Earth’s atmosphere. However, there is currently no consensus on when and how oxygenic photosynthesis originated. Here we present a Bayesian relaxed molecular clock analysis of the two core subunits of Photosystem II, D1 and D2, to study the origin of water oxidation. We timed the phylogeny of Type II reaction center proteins using geochemical constraints and calibrations derived from the fossil record of Cyanobacteria and photosynthetic eukaryotes. Age estimates were interpreted in the context of the structure and function of photochemical reaction centers. Firstly, we point out that the ancestral protein to D1 and D2 gave rise to a homodimeric photosystem that was capable of water oxidation, although less efficiently and by a different mechanism than the well-characterized oxygen evolving complex. Secondly, our results indicate that the gene duplication event that led to the divergence of D1 and D2 is likely to have occurred more than a billion years before the last common ancestor of Cyanobacteria. Thirdly, we show that Cyanobacteria did not obtain Type II reaction centers via horizontal gene transfer. Furthermore, the data suggests that the origin of photosynthesis in the early Archaean was necessarily followed by a rapid diversification of all the families of reaction center proteins, which included the divergence of D1 and D2. Our analysis suggests that primordial forms of water oxidation originated relatively soon after the emergence of photochemical reaction centers in the early Archaean.