Relative stability of the S 2 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. Gunner

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish
JournalPhotosynthesis Research
DOIs
Publication statusPublished - Jan 1 2019

Fingerprint

oxygen evolving complex
Photosystem II Protein Complex
Isomers
photosystem II
isomers
Oxygen
Protonation
Oxidation-Reduction
Water
oxidation
water
Oxidation
protons
Protons
Chlorides
energy
chlorides
Ligands
mutants
Deprotonation

Keywords

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

ASJC Scopus subject areas

  • Biochemistry
  • Plant Science
  • Cell Biology

Cite this

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

In: Photosynthesis Research, 01.01.2019.

Research output: Contribution to journalArticle

Kaur, D, Szejgis, W, Mao, J, Amin, M, Reiss, KM, Askerka, M, Cai, X, Khaniya, U, Zhang, Y, Brudvig, GW, Batista, VS & Gunner, MR 2019, ' Relative stability of the S 2 isomers of the oxygen evolving complex of photosystem II ', Photosynthesis Research. https://doi.org/10.1007/s11120-019-00637-6
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. / Relative stability of the S 2 isomers of the oxygen evolving complex of photosystem II In: Photosynthesis Research. 2019.
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abstract = "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.",
keywords = "Grand canonical Monte Carlo simulations, Linear response approximation (LRA), Oxygen evolving complex (OEC), Photosystem II, pK, Proton transfer",
author = "Divya Kaur and Witold Szejgis and Junjun Mao and Muhamed Amin and Reiss, {Krystle M.} and Mikhail Askerka and Xiuhong Cai and Umesh Khaniya and Yingying Zhang and Brudvig, {Gary W} and Batista, {Victor S.} and Gunner, {M. R.}",
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AU - Kaur, Divya

AU - Szejgis, Witold

AU - Mao, Junjun

AU - Amin, Muhamed

AU - Reiss, Krystle M.

AU - Askerka, Mikhail

AU - Cai, Xiuhong

AU - Khaniya, Umesh

AU - Zhang, Yingying

AU - Brudvig, Gary W

AU - Batista, Victor S.

AU - Gunner, M. R.

PY - 2019/1/1

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N2 - 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.

AB - 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.

KW - Grand canonical Monte Carlo simulations

KW - Linear response approximation (LRA)

KW - Oxygen evolving complex (OEC)

KW - Photosystem II

KW - pK

KW - Proton transfer

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