Photosynthesis Research

, Volume 141, Issue 3, pp 331–341 | Cite as

Relative stability of the S2 isomers of the oxygen evolving complex of photosystem II

  • Divya Kaur
  • Witold Szejgis
  • Junjun Mao
  • Muhamed Amin
  • Krystle M. Reiss
  • Mikhail Askerka
  • Xiuhong Cai
  • Umesh Khaniya
  • Yingying Zhang
  • Gary W. Brudvig
  • Victor S. Batista
  • M. R. GunnerEmail author
Original Article


The oxidation of water to O2 is catalyzed by the Oxygen Evolving Complex (OEC), a Mn4CaO5 complex in Photosystem II (PSII). The OEC is sequentially oxidized from state S0 to S4. The S2 state, (MnIII)(MnIV)3, coexists in two redox isomers: S2,g=2, where Mn4 is MnIV and S2,g=4.1, where Mn1 is MnIV. Mn4 has two terminal water ligands, whose proton affinity is affected by the Mn oxidation state. The relative energy of the two S2 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 S1 and S2 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 YZ/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 S2,g=2 redox isomer is the lower energy state; while chloride depletion or pH 8 stabilizes the S2,g=4.1 state and the mutants D2-K317A, D1-D61A, and D1-S169A favor the S2,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 S2,g=2 state, indicating the two water protonation states have similar energy, while it remains neutral in the S1 and S2,g=4.1 states. In wild-type PSII, advancement to S2 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 S2 state.


Grand canonical Monte Carlo simulations Linear response approximation (LRA) Oxygen evolving complex (OEC) pKa Photosystem II Proton transfer 



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.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11120_2019_637_MOESM1_ESM.pdf (1.1 mb)
Supplementary material 1 (PDF 1165 KB)


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Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of ChemistryThe Graduate Center of the City University of New YorkNew YorkUSA
  2. 2.Department of PhysicsCity College of New YorkNew YorkUSA
  3. 3.University of GroningenGroningenThe Netherlands
  4. 4.Department of ChemistryYale UniversityNew HavenUSA
  5. 5.Department of PhysicsThe Graduate Center of the City University of New YorkNew YorkUSA

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