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 new perspective on the evolution of oxygenic photosynthesis by studying the evolution of D1 and D2, the core subunits of Photosystem II, as a function of time. A Bayesian relaxed molecular clock approach was applied to the phylogeny of Type II reaction center proteins using geochemical constraints and calibrations derived from the fossil record of Cyanobacteria and photosynthetic eukaryotes. The resulting age estimates were interpreted in the context of the structure and function of photochemical reaction centers. Firstly, we point out it is likely that the ancestral protein to D1 and D2 gave rise to a photosystem that was capable of water oxidation. 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 emergence of the last common ancestor of extant Cyanobacteria. Thirdly, we show that it is unlikely that Cyanobacteria obtained photosynthesis via horizontal gene transfer. Furthermore, the data strongly suggest that the origin of photosynthesis in the early Archaean was necessarily followed by a rapid diversification of reaction center proteins, which included the divergence of D1 and D2. It is therefore concluded that primordial forms of water oxidation could have originated relatively soon after the emergence of photosynthesis.
