Occupancy Analysis of Water Molecules inside Channels within 25 Å Radius of the Oxygen-Evolving Center of Photosystem II in Molecular Dynamics Simulations

Abstract

At room temperature and neutral pH, the oxygen-evolving center (OEC) of photosystem II (PSII) catalyzes water oxidation. During this process, oxygen is released from the OEC, while substrate waters are delivered to the OEC and protons are passed from the OEC to the lumen through water channels known as the narrow or the O4 channel, broad or the Cl1 channel, and large or the O1 channel. Protein residues lining the surfaces of these channels play a critical role in stabilizing the hydrogen-bonding networks that assist in the process. We carried out an occupancy analysis to better understand the structural and possible substrate water dynamics in full PSII monomer molecular dynamics (MD) trajectories in both the S 1 and S 2 states. We find that the equilibrated positions of water molecules derived from MD-derived electron density maps largely match the experimentally observed positions in crystallography. Furthermore, the occupancy reduction in MD simulations of some water molecules inside the single-filed narrow channel also correlates well with the crystallographic data during a structural transition when the S 1 state of the OEC advances to the S 2 state. The overall reduced occupancies of water molecules are the source of their "vacancy-hopping" dynamic nature inside these channels, unlike water molecules inside an ice lattice where all water molecules have a fixed unit occupancy. We propose on the basis of findings in our structural and molecular dynamics analysis that the water molecule occupying a pocket formed by D1-D61, D1-S169, and O4 of the OEC could be the last steppingstone to enter into the OEC and that the broad channel may be favored for proton transfer.

Bioinspired Water Preorganization in Confined Space for Efficient Water Oxidation Catalysis in Metallosupramolecular Ruthenium Architectures

“…The high proton mobility in water results from proton migration through an ordered hydrogen-bonded water network according to the Grotthuss mechanism . Reminiscent of natural enzymatic pockets, supramolecular preorganization of small molecules can be promoted by the molecular design of confined environments .…”

“…The high proton mobility in water results from proton migration through an ordered hydrogen-bonded water network according to the Grotthuss mechanism. 33 Reminiscent of natural enzymatic pockets, supramolecular preorganization of small molecules can be promoted by the molecular design of confined environments. 34 In the field of water oxidation catalysis, initial approaches mainly focused on accelerating the bimolecular intercatalyst coupling of the I2M pathway via encapsulation of mononuclear Ru WOCs into supramolecular nanocages, 35 while reports on macrocyclic Ru WOCs were rather scarce prior to our first report.…”

Independent Mutation of Two Bridging Carboxylate Ligands Stabilizes Alternate Conformers of the Photosynthetic O2-Evolving Mn4CaO5 Cluster in Photosystem II

“…Proton egress and substrate water access are facilitated by extensive networks of H-bonds that make up three well-defined pathways that connect the Mn 4 CaO 5 cluster with the thylakoid lumen. These are known as the O1, O4, and Cl1 pathways because of where they appear to originate on or near the Mn 4 CaO 5 cluster (for recent descriptions of these pathways, see refs – ).…”