The S₂ State of the Oxygen‐Evolving Complex of Photosystem II Explored by QM/MM Dynamics: Spin Surfaces and Metastable States Suggest a Reaction Path Towards the S₃ State

Abstract

# These authors contributed equally to this work. Keywords ab initio calculations; density functional calculations; Kok cycle; photosystem II; water splittingOne of the key steps in photosynthetic solar-energy conversion performed by plants, algae, and cyanobacteria is the splitting of water into molecular oxygen and hydrogen equivalents. [1] To achieve this challenging task photosynthetic organisms use a protein complex that remained almost unchanged during the evolution in the last two and a half billion years: the photosystem II (PSII). The reaction proceeds by the accumulation of four oxidizing equivalents on the {Mn 4 CaO 5 } cluster through five (S 0 -S 4 ) oxidation states that are sequentially attained during water splitting (Kok cycle). [2] The deep understanding of the way nature has found to perform this difficult task efficiently has a great relevance not only for biology but also for inspiring the development of biomimetic artificial systems that can be used to store solar energy in an environmentally friendly way. [3] Atomic details of the structure of the oxygen-evolving complex (OEC) of PSII have been revealed by extended Xray absorption fine structure (EXAFS) experiments and by X-ray crystallography at increasing resolution levels. [4] However, the accurate position of the {Mn 4 CaO 5 } cluster atoms and its ligands emerged only when a X-ray structure at 1.9 Å resolution became accessible. [5] However, the effect of a possible X-ray photo-reduction, in particular on the characterization of the Kok's state described by this structure and on the unrealistic bond lengths between the oxygen atom O5 and the two manganese ions Mn1 and Mn4, is matter of debate. [6] Additionally, important contributions to the structure refinement came from theoretical studies. [6b,7] Apart from a detailed characterization of the molecular structure of the OEC, an exact description of the water-splitting catalytic mechanism cannot leave aside an accurate

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn 4 CaO 5 cluster in photosystem II

“…In the S 2 state, Mn 1 or Mn 4 was oxidized in the high-oxidation models, whereas Mn 2 or Mn 4 was oxidized in the low-oxidation models. The Mn 1 -and Mn 4 -oxidized S 2 states of the high-oxidation models have been proposed to reflect two conformations showing g = 4.1 and g = 2 multiline EPR signals, respectively, where the latter conformation has a slightly lower energy (10,14,17).…”

“…It is, thus, possible that the W3 and W4 attached to Ca 2+ are involved in proton release in water oxidation, especially during the S 2 →S 3 transition, which is inhibited by Ca 2+ depletion (53). It has also been proposed that W3 moves to Mn 4 during the S 2 →S 3 transition in the so-called oxo-oxyl mechanism (13,17,22). Thus, the carboxylate ligands bridging Mn and Ca ions may play an important role in water oxidation by tuning the reactivity of water ligands on Ca by charge shifts via their π conjugation.…”

“…High-spin states were assumed in calculations. The protonation states of W2 and O5 were assumed to be H 2 O, OH − , or O 2− following previous studies (10,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24).…”

“…With the information of atomic coordinates from high-resolution X-ray structures of the WOC, quantum chemical calculation is now a very powerful method in investigation of the water oxidation mechanism (10,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24). Calculations using the density functional theory (DFT) and quantum mechanics/molecular mechanics (QM/MM) methods can be used to predict individual S-state structures and hence, the reaction scheme.…”

Pathway for Mn-cluster oxidation by tyrosine-Z in the S 2 state of photosystem II

“…1), can explain the presence of the two distinct EPR signals revealed at cryogenic temperatures (i.e., a multiline signal indicative of a ground state characterized by a spin S = 1/2 and a second signal at g = 4.1 consistent with a spin S = 5/2). In a recent work (37) we characterized by extensive quantum mechanics/molecular mechanics (QM/MM) ab initio simulations the free-energy profiles for the interconversion between the two abovementioned conformations, suggesting that the transition from the S 2 to S 3 state should proceed passing first by the S A 2 and subsequently through the S B 2 state. Still, clear evidence confirming such a hypothesis is missing.…”