Fourier transform infrared detection of a polarizable proton trapped between photooxidized tyrosine YZ and a coupled histidine in photosystem II: Relevance to the proton transfer mechanism of water oxidation

Shin Nakamura, Ryo Nagao, Ryouta Takahashi, Takumi Noguchi

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Abstract

The redox-active tyrosine YZ (D1-Tyr161) in photosystem II (PSII) functions as an immediate electron acceptor of the Mn4Ca cluster, which is the catalytic center of photosynthetic water oxidation. Y Z is also located in the hydrogen bond network that connects the Mn4Ca cluster to the lumen and hence is possibly related to the proton transfer process during water oxidation. To understand the role of Y Z in the water oxidation mechanism, we have studied the hydrogen bonding interactions of YZ and its photooxidized neutral radical YZ together with the interaction of the coupled His residue, D1-His190, using light-induced Fourier transform infrared (FTIR) difference spectroscopy. The YZ -minus-YZ FTIR difference spectrum of Mn-depleted PSII core complexes exhibited a broad positive feature around 2800 cm-1, which was absent in the corresponding spectrum of another redox-active tyrosine YD (D2-Tyr160). Analyses by 15N and H/D substitutions, examination of the pH dependence, and density functional theory and quantum mechanics/molecular mechanics (QM/MM) calculations showed that this band arises from the N-H stretching vibration of the protonated cation of D1-His190 forming a charge-assisted strong hydrogen bond with YZ . This result provides strong evidence that the proton released from YZ upon its oxidation is trapped in D1-His190 and a positive charge remains on this His. The broad feature of the ∼2800 cm-1 band reflects a large proton polarizability in the hydrogen bond between YZ and HisH+. QM/MM calculations further showed that upon YZ oxidation the hydrogen bond network is rearranged and one water molecule moves toward D1-His190. From these data, a novel proton transfer mechanism via YZ -HisH+ is proposed, in which hopping of the polarizable proton of HisH+ to this water triggers the transfer of the proton from substrate water to the luminal side. This proton transfer mechanism could be functional in the S2 → S3 transition, which requires proton release before electron transfer because of an excess positive charge on the Mn4Ca cluster.

Original languageEnglish
Pages (from-to)3131-3144
Number of pages14
JournalBiochemistry
Volume53
Issue number19
DOIs
Publication statusPublished - May 20 2014
Externally publishedYes

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Proton transfer
Photosystem II Protein Complex
Fourier Analysis
Histidine
Tyrosine
Protons
Fourier transforms
Hydrogen bonds
Infrared radiation
Oxidation
Water
Mechanics
Hydrogen
Molecular mechanics
Quantum theory
Oxidation-Reduction
Electrons
Quantum Theory
Electron transitions
Stretching

ASJC Scopus subject areas

  • Biochemistry

Cite this

@article{8d6dface8d9544b59867857a83b75fde,
title = "Fourier transform infrared detection of a polarizable proton trapped between photooxidized tyrosine YZ and a coupled histidine in photosystem II: Relevance to the proton transfer mechanism of water oxidation",
abstract = "The redox-active tyrosine YZ (D1-Tyr161) in photosystem II (PSII) functions as an immediate electron acceptor of the Mn4Ca cluster, which is the catalytic center of photosynthetic water oxidation. Y Z is also located in the hydrogen bond network that connects the Mn4Ca cluster to the lumen and hence is possibly related to the proton transfer process during water oxidation. To understand the role of Y Z in the water oxidation mechanism, we have studied the hydrogen bonding interactions of YZ and its photooxidized neutral radical YZ • together with the interaction of the coupled His residue, D1-His190, using light-induced Fourier transform infrared (FTIR) difference spectroscopy. The YZ •-minus-YZ FTIR difference spectrum of Mn-depleted PSII core complexes exhibited a broad positive feature around 2800 cm-1, which was absent in the corresponding spectrum of another redox-active tyrosine YD (D2-Tyr160). Analyses by 15N and H/D substitutions, examination of the pH dependence, and density functional theory and quantum mechanics/molecular mechanics (QM/MM) calculations showed that this band arises from the N-H stretching vibration of the protonated cation of D1-His190 forming a charge-assisted strong hydrogen bond with YZ •. This result provides strong evidence that the proton released from YZ upon its oxidation is trapped in D1-His190 and a positive charge remains on this His. The broad feature of the ∼2800 cm-1 band reflects a large proton polarizability in the hydrogen bond between YZ • and HisH+. QM/MM calculations further showed that upon YZ oxidation the hydrogen bond network is rearranged and one water molecule moves toward D1-His190. From these data, a novel proton transfer mechanism via YZ •-HisH+ is proposed, in which hopping of the polarizable proton of HisH+ to this water triggers the transfer of the proton from substrate water to the luminal side. This proton transfer mechanism could be functional in the S2 → S3 transition, which requires proton release before electron transfer because of an excess positive charge on the Mn4Ca cluster.",
author = "Shin Nakamura and Ryo Nagao and Ryouta Takahashi and Takumi Noguchi",
year = "2014",
month = "5",
day = "20",
doi = "10.1021/bi500237y",
language = "English",
volume = "53",
pages = "3131--3144",
journal = "Biochemistry",
issn = "0006-2960",
publisher = "American Chemical Society",
number = "19",

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TY - JOUR

T1 - Fourier transform infrared detection of a polarizable proton trapped between photooxidized tyrosine YZ and a coupled histidine in photosystem II

T2 - Relevance to the proton transfer mechanism of water oxidation

AU - Nakamura, Shin

AU - Nagao, Ryo

AU - Takahashi, Ryouta

AU - Noguchi, Takumi

PY - 2014/5/20

Y1 - 2014/5/20

N2 - The redox-active tyrosine YZ (D1-Tyr161) in photosystem II (PSII) functions as an immediate electron acceptor of the Mn4Ca cluster, which is the catalytic center of photosynthetic water oxidation. Y Z is also located in the hydrogen bond network that connects the Mn4Ca cluster to the lumen and hence is possibly related to the proton transfer process during water oxidation. To understand the role of Y Z in the water oxidation mechanism, we have studied the hydrogen bonding interactions of YZ and its photooxidized neutral radical YZ • together with the interaction of the coupled His residue, D1-His190, using light-induced Fourier transform infrared (FTIR) difference spectroscopy. The YZ •-minus-YZ FTIR difference spectrum of Mn-depleted PSII core complexes exhibited a broad positive feature around 2800 cm-1, which was absent in the corresponding spectrum of another redox-active tyrosine YD (D2-Tyr160). Analyses by 15N and H/D substitutions, examination of the pH dependence, and density functional theory and quantum mechanics/molecular mechanics (QM/MM) calculations showed that this band arises from the N-H stretching vibration of the protonated cation of D1-His190 forming a charge-assisted strong hydrogen bond with YZ •. This result provides strong evidence that the proton released from YZ upon its oxidation is trapped in D1-His190 and a positive charge remains on this His. The broad feature of the ∼2800 cm-1 band reflects a large proton polarizability in the hydrogen bond between YZ • and HisH+. QM/MM calculations further showed that upon YZ oxidation the hydrogen bond network is rearranged and one water molecule moves toward D1-His190. From these data, a novel proton transfer mechanism via YZ •-HisH+ is proposed, in which hopping of the polarizable proton of HisH+ to this water triggers the transfer of the proton from substrate water to the luminal side. This proton transfer mechanism could be functional in the S2 → S3 transition, which requires proton release before electron transfer because of an excess positive charge on the Mn4Ca cluster.

AB - The redox-active tyrosine YZ (D1-Tyr161) in photosystem II (PSII) functions as an immediate electron acceptor of the Mn4Ca cluster, which is the catalytic center of photosynthetic water oxidation. Y Z is also located in the hydrogen bond network that connects the Mn4Ca cluster to the lumen and hence is possibly related to the proton transfer process during water oxidation. To understand the role of Y Z in the water oxidation mechanism, we have studied the hydrogen bonding interactions of YZ and its photooxidized neutral radical YZ • together with the interaction of the coupled His residue, D1-His190, using light-induced Fourier transform infrared (FTIR) difference spectroscopy. The YZ •-minus-YZ FTIR difference spectrum of Mn-depleted PSII core complexes exhibited a broad positive feature around 2800 cm-1, which was absent in the corresponding spectrum of another redox-active tyrosine YD (D2-Tyr160). Analyses by 15N and H/D substitutions, examination of the pH dependence, and density functional theory and quantum mechanics/molecular mechanics (QM/MM) calculations showed that this band arises from the N-H stretching vibration of the protonated cation of D1-His190 forming a charge-assisted strong hydrogen bond with YZ •. This result provides strong evidence that the proton released from YZ upon its oxidation is trapped in D1-His190 and a positive charge remains on this His. The broad feature of the ∼2800 cm-1 band reflects a large proton polarizability in the hydrogen bond between YZ • and HisH+. QM/MM calculations further showed that upon YZ oxidation the hydrogen bond network is rearranged and one water molecule moves toward D1-His190. From these data, a novel proton transfer mechanism via YZ •-HisH+ is proposed, in which hopping of the polarizable proton of HisH+ to this water triggers the transfer of the proton from substrate water to the luminal side. This proton transfer mechanism could be functional in the S2 → S3 transition, which requires proton release before electron transfer because of an excess positive charge on the Mn4Ca cluster.

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