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

• Published in: Photosynthesis research 2019-09, Vol.141 (3), p.331-341
• 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: Biochemistry; Biomedical and Life Sciences; Chlorides; Electrostatic properties; Energy; Isomers; Life Sciences; Ligands; Original Article; Oxidation; Oxygen; pH effects; Photosystem II; Plant Genetics and Genomics; Plant Physiology; Plant Sciences
• ISSN: 0166-8595; 1573-5079
• DOI: 10.1007/s11120-019-00637-6

The oxidation of water to O 2 is catalyzed by the Oxygen Evolving Complex (OEC), a Mn 4 CaO 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.