Structural and dynamic insights into Mn4Ca cluster-depleted Photosystem II

In the first steps of natural oxygenic photosynthesis, sunlight is used to oxidize water molecules to protons, electrons and molecular oxygen. This reaction takes place on the Mn4Ca cluster located in the reaction centre of Photosystem II (PSII), where the cluster is assembled and continuously repaired through a process known as photoactivation. Understanding the molecular details of such a process has important implications in different fields, in particular inspiring synthesis and repair strategies for artificial photosynthesis devices. In this regard, a detailed structural and dynamic characterization of Photosystem II lacking a Mn4Ca cluster, namely apo PSII, is a prerequisite for the full comprehension of the photoactivation. Recently, the structure of the apo PSII was resolved at 2.55 angstrom resolution [Zhang et al., eLife, 2017, 6, e26933], suggesting a pre-organized structure of the protein cavity hosting the cluster. Anyway, the question of whether these findings are a feature of the method used remains open. Here, by means of classical Molecular Dynamics simulations, we characterized the structural and dynamic features of the apo PSII for different protonation states of the cluster cavity. Albeit an overall conformational stability common to all investigated systems, we found significant deviations in the conformation of the side chains of the active site with respect to the X-ray positions. Our findings suggest that not all residues acting as Mn ligands are pre-organized prior to the Mn4Ca formation and previous local conformational changes are required in order to bind the first Mn ion in the high-affinity binding site.