No abstract

Structural dynamics of water and its hydrogen-bonding networks play an important role in enzyme function via the transport of protons, ions, and substrates. To gain insights into these mechanisms in the water oxidation reaction in Photosystem II (PS II), we have performed crystalline molecular dynamics (MD) simulations of the dark-stable S 1 state. Our MD model consists of a full unit cell with 8 PS II monomers in explicit solvent (861 894 atoms), enabling us to compute the simulated crystalline electron density and to compare it directly with the experimental density from serial femtosecond X-ray crystallography under physiological temperature collected at X-ray free electron lasers (XFELs). The MD density reproduced the experimental density and water positions with high fidelity. The detailed dynamics in the simulations provided insights into the mobility of water molecules in the channels beyond what can be interpreted from experimental B-factors and electron densities alone. In particular, the simulations revealed fast, coordinated exchange of waters at sites where the density is strong, and water transport across the bottleneck region of the channels where the density is weak. By computing MD hydrogen and oxygen maps separately, we developed a novel Map-based Acceptor−Donor Identification (MADI) technique that yields information which helps to infer hydrogen-bond directionality and strength. The MADI analysis revealed a series of hydrogen-bond wires emanating from the Mn cluster through the Cl1 and O4 channels; such wires might provide pathways for proton transfer during the reaction cycle of PS II. Our simulations provide an atomistic picture of the dynamics of water and hydrogen-bonding networks in PS II, with implications for the specific role of each channel in the water oxidation reaction.

Photosystem II (PSII) of plants, algae and cyanobacteria is a specialised protein complex that uses light energy to transfer electrons from water to plastoquinone, producing molecular oxygen and reduced plastoquinone. The PSII complex includes a peripheral antenna containing chlorophyll and other pigments to absorb light, a reaction centre that utilises the excitation energy transferred to it for charge separation, cofactors that stabilise the charge pair via electron transfer reactions, a Mn 4 CaO 5 cluster that oxidises water, and a binding pocket where plastoquinone is reduced. The electrons and protons that PSII extracts from water are employed in the overall photosynthetic process for the reduction of CO 2 , which provides the chemical energy for most life on Earth. PSII is the only known biological source of O 2 produced from water and is responsible for the molecular oxygen in the atmosphere. Key Concepts Photosystem II (PSII) is a membrane‐embedded pigment–protein complex, containing more than 20 subunits and approximately 100 cofactors. The PSII antenna and the PSII reaction centre are distinct protein complexes. Light is absorbed by chlorophyll, carotenoid and phycobilin pigments in the antenna and the excitation energy is rapidly transferred to the reaction centre. At the reaction centre, light‐induced charge separation takes place resulting in the formation of a chlorophyll cation and a pheophytin anion that are approximately 10 Å apart; this charge separation is rapidly stabilised by the transfer of the charges to more distant cofactors with smaller differences in redox potentials. The oxidation of water occurs at the Mn 4 CaO 5 cluster, which is embedded in the two protein subunits D1 and CP43 on the luminal side of PSII. To oxidise two molecules of water, four oxidising equivalents must be accumulated in the Mn 4 CaO 5 cluster by four consecutive light‐induced charge separations. Water oxidation by PSII occurs at the Mn 4 CaO 5 cluster, likely via oxo‐oxyl radical coupling in the so‐called S 4 state. Hydrogen‐bonding networks surrounding the Mn 4 CaO 5 cluster are crucial for its catalytic activity, as well as its structural flexibility. Bicarbonate ions play regulatory roles for electron transfer through PSII. The electrons and protons extracted from water by PSII drive the reduction of NADP + via Photosystem I, and the production of ATP, respectively.

No abstract