Relative stability of the S 2 isomers of the oxygen evolving complex of photosystem II

• Published in: Photosynthesis research 2019-09, Vol.141 (3), p.331
• Main Authors: Kaur, Divya, Szejgis, Witold, Mao, Junjun, Amin, Muhamed, Reiss, Krystle M, Askerka, Mikhail, Cai, Xiuhong, Khaniya, Umesh, Zhang, Yingying, Brudvig, Gary W, Batista, Victor S, Gunner, M R
• Format: Article
• Language: English
• Subjects: Chlorides - metabolism; Hydrogen-Ion Concentration; Isomerism; Ligands; Models, Molecular; Mutagenesis; Mutation - genetics; Oxidation-Reduction; Oxygen - metabolism; Photosystem II Protein Complex - chemistry; Photosystem II Protein Complex - metabolism; Protein Stability; Protons; Water - metabolism
• ISSN: 1573-5079
• DOI: 10.1007/s11120-019-00637-6

The oxidation of water to O is catalyzed by the Oxygen Evolving Complex (OEC), a Mn CaO complex in Photosystem II (PSII). The OEC is sequentially oxidized from state S to S . The S state, (Mn )(Mn ) , coexists in two redox isomers: S , where Mn4 is Mn and S , where Mn1 is Mn . Mn4 has two terminal water ligands, whose proton affinity is affected by the Mn oxidation state. The relative energy of the two S redox isomers and the protonation state of the terminal water ligands are analyzed using classical multi-conformer continuum electrostatics (MCCE). The Monte Carlo simulations are done on QM/MM optimized S and S structures docked back into the complete PSII, keeping the protonation state of the protein at equilibrium with the OEC redox and protonation states. Wild-type PSII, chloride-depleted PSII, PSII in the presence of oxidized Y /protonated D1-H190, and the PSII mutants D2-K317A, D1-D61A, and D1-S169A are studied at pH 6. The wild-type PSII at pH 8 is also described. In qualitative agreement with experiment, in wild-type PSII, the S redox isomer is the lower energy state; while chloride depletion or pH 8 stabilizes the S state and the mutants D2-K317A, D1-D61A, and D1-S169A favor the S state. The protonation states of D1-E329, D1-E65, D1-H337, D1-D61, and the terminal waters on Mn4 (W1 and W2) are affected by the OEC oxidation state. The terminal W2 on Mn4 is a mixture of water and hydroxyl in the S state, indicating the two water protonation states have similar energy, while it remains neutral in the S and S states. In wild-type PSII, advancement to S leads to negligible proton loss and so there is an accumulation of positive charge. In the analyzed mutations and Cl depleted PSII, additional deprotonation is found upon formation of S state.