Relative stability of the S 2 isomers of the oxygen evolving complex of photosystem II Original Article First Online: 02 April 2019 Abstract
The oxidation of water to O
2 is catalyzed by the Oxygen Evolving Complex (OEC), a Mn 4CaO 5 complex in Photosystem II (PSII). The OEC is sequentially oxidized from state S 0 to S 4. The S 2 state, (Mn III)(Mn IV) 3, coexists in two redox isomers: S 2,g=2, where Mn4 is Mn IV and S 2,g=4.1, where Mn1 is Mn IV. Mn4 has two terminal water ligands, whose proton affinity is affected by the Mn oxidation state. The relative energy of the two S 2 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 1 and S 2 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 Z/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 2,g=2 redox isomer is the lower energy state; while chloride depletion or pH 8 stabilizes the S 2,g=4.1 state and the mutants D2-K317A, D1-D61A, and D1-S169A favor the S 2,g=2 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 2,g=2 state, indicating the two water protonation states have similar energy, while it remains neutral in the S 1 and S 2,g=4.1 states. In wild-type PSII, advancement to S 2 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 2 state. Keywords Grand canonical Monte Carlo simulations Linear response approximation (LRA) Oxygen evolving complex (OEC) pK a Photosystem II Proton transfer Electronic supplementary material
The online version of this article (
) contains supplementary material, which is available to authorized users. https://doi.org/10.1007/s11120-019-00637-6 Notes Acknowledgements
We would like to thank David Vinyard for very helpful discussion. We acknowledge financial support from the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences, U.S. Department of Energy, Photosynthetic Systems. Experimental work was funded by DE-FG02-05ER15646 (G. W. B.) and computational studies by DESC0001423 (M. R. G. and V. S. B.). M. R. G. also acknowledges infrastructure support from the National Institute on Minority Health and Health Disparities (Grant 8G12MD007603) from the National Institutes of Health. V. S. B. acknowledges DOE high-performance computing time from NERSC.
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