Evidence that D1-His332 in photosystem II from Thermosynechococcus elongatus interacts with the S3-state and not with the S2-state

Miwa Sugiura; Fabrice Rappaport; Warwick Hillier; Pierre Dorlet; Yohei Ohno; Hidenori Hayashi; Alain Boussac

doi:10.1021/bi901067b

Evidence that D1-His332 in photosystem II from Thermosynechococcus elongatus interacts with the S3-state and not with the S2-state

Miwa Sugiura^*, Fabrice Rappaport, Warwick Hillier, Pierre Dorlet, Yohei Ohno, Hidenori Hayashi, Alain Boussac

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

18 Citations (Scopus)

Abstract

Oxygen evolution by Photosystem II (PSII) is catalyzed by a Mn ₄Ca cluster. Thus far, from the crystallographic three-dimensional (3D) structures, seven amino acid residues have been identified as possible ligands of the Mn₄Ca cluster. Among them, there is only one histidine, His332, which belongs to the D1 polypeptide. The relationships of the D1-His332 amino acid with kinetics and thermodynamic properties of the Mn ₄Ca cluster in the S₂- and S₃-states of the catalytic cycle were investigated in purified PSII from Thermosynechococcus elongatus. This was done by examining site-directed D1-His332Gln and D1-His332Ser mutants by a variety of spectroscopic techniques such as time-resolved UV-visible absorption change spectroscopy, cw- and pulse-EPR, thermoluminescence, and measurement of substrate water exchange. Both mutants grew photo-autotrophically and active PSII could be purified. On the basis of the parameters assessed in this work, the D1-His332(Gln, Ser) mutations had no effect in the S₂-state. Electron spin-echo envelope modulation (ESEEM) spectroscopy also showed that possible interactions between the nuclear spin of the nitrogen(s) of D1-His332 with the electronic spin S = 1/2 of the Mn₄Ca cluster in the S₂-state were not detectable and that the D1-His332Ser mutation did not affect the detected hyperfine couplings. In contrast, the following changes were observed in the S₃-state of the D1-His332 mutants: (1) The redox potential of the S₃/S₂ couple was slightly increased by ≤20 meV, (2) The S₃-EPR spectrum was slightly modified, (3) The D1-His332Gln mutation resulted in a ∼3 fold decrease of the slow (tightly bound) exchange rate and a ∼2 fold increase of the fast exchange rate of the water substrate molecules. All these results suggest that the D1-His332 would be more involved in S₃ than in S₂. This could be one element of the conformational changes put forward in the S₂ to S₃ transition.

Original language	English
Pages (from-to)	7856-7866
Number of pages	11
Journal	Biochemistry
Volume	48
Issue number	33
DOIs	https://doi.org/10.1021/bi901067b
Publication status	Published - 25 Aug 2009

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@article{05d981cba188448eafc2a252fc9895ec,

title = "Evidence that D1-His332 in photosystem II from Thermosynechococcus elongatus interacts with the S3-state and not with the S2-state",

abstract = "Oxygen evolution by Photosystem II (PSII) is catalyzed by a Mn 4Ca cluster. Thus far, from the crystallographic three-dimensional (3D) structures, seven amino acid residues have been identified as possible ligands of the Mn4Ca cluster. Among them, there is only one histidine, His332, which belongs to the D1 polypeptide. The relationships of the D1-His332 amino acid with kinetics and thermodynamic properties of the Mn 4Ca cluster in the S2- and S3-states of the catalytic cycle were investigated in purified PSII from Thermosynechococcus elongatus. This was done by examining site-directed D1-His332Gln and D1-His332Ser mutants by a variety of spectroscopic techniques such as time-resolved UV-visible absorption change spectroscopy, cw- and pulse-EPR, thermoluminescence, and measurement of substrate water exchange. Both mutants grew photo-autotrophically and active PSII could be purified. On the basis of the parameters assessed in this work, the D1-His332(Gln, Ser) mutations had no effect in the S2-state. Electron spin-echo envelope modulation (ESEEM) spectroscopy also showed that possible interactions between the nuclear spin of the nitrogen(s) of D1-His332 with the electronic spin S = 1/2 of the Mn4Ca cluster in the S2-state were not detectable and that the D1-His332Ser mutation did not affect the detected hyperfine couplings. In contrast, the following changes were observed in the S3-state of the D1-His332 mutants: (1) The redox potential of the S3/S2 couple was slightly increased by ≤20 meV, (2) The S3-EPR spectrum was slightly modified, (3) The D1-His332Gln mutation resulted in a ∼3 fold decrease of the slow (tightly bound) exchange rate and a ∼2 fold increase of the fast exchange rate of the water substrate molecules. All these results suggest that the D1-His332 would be more involved in S3 than in S2. This could be one element of the conformational changes put forward in the S2 to S3 transition.",

author = "Miwa Sugiura and Fabrice Rappaport and Warwick Hillier and Pierre Dorlet and Yohei Ohno and Hidenori Hayashi and Alain Boussac",

year = "2009",

month = aug,

day = "25",

doi = "10.1021/bi901067b",

language = "English",

volume = "48",

pages = "7856--7866",

journal = "Biochemistry",

issn = "0006-2960",

publisher = "American Chemical Society",

number = "33",

}

TY - JOUR

T1 - Evidence that D1-His332 in photosystem II from Thermosynechococcus elongatus interacts with the S3-state and not with the S2-state

AU - Sugiura, Miwa

AU - Rappaport, Fabrice

AU - Hillier, Warwick

AU - Dorlet, Pierre

AU - Ohno, Yohei

AU - Hayashi, Hidenori

AU - Boussac, Alain

PY - 2009/8/25

Y1 - 2009/8/25

N2 - Oxygen evolution by Photosystem II (PSII) is catalyzed by a Mn 4Ca cluster. Thus far, from the crystallographic three-dimensional (3D) structures, seven amino acid residues have been identified as possible ligands of the Mn4Ca cluster. Among them, there is only one histidine, His332, which belongs to the D1 polypeptide. The relationships of the D1-His332 amino acid with kinetics and thermodynamic properties of the Mn 4Ca cluster in the S2- and S3-states of the catalytic cycle were investigated in purified PSII from Thermosynechococcus elongatus. This was done by examining site-directed D1-His332Gln and D1-His332Ser mutants by a variety of spectroscopic techniques such as time-resolved UV-visible absorption change spectroscopy, cw- and pulse-EPR, thermoluminescence, and measurement of substrate water exchange. Both mutants grew photo-autotrophically and active PSII could be purified. On the basis of the parameters assessed in this work, the D1-His332(Gln, Ser) mutations had no effect in the S2-state. Electron spin-echo envelope modulation (ESEEM) spectroscopy also showed that possible interactions between the nuclear spin of the nitrogen(s) of D1-His332 with the electronic spin S = 1/2 of the Mn4Ca cluster in the S2-state were not detectable and that the D1-His332Ser mutation did not affect the detected hyperfine couplings. In contrast, the following changes were observed in the S3-state of the D1-His332 mutants: (1) The redox potential of the S3/S2 couple was slightly increased by ≤20 meV, (2) The S3-EPR spectrum was slightly modified, (3) The D1-His332Gln mutation resulted in a ∼3 fold decrease of the slow (tightly bound) exchange rate and a ∼2 fold increase of the fast exchange rate of the water substrate molecules. All these results suggest that the D1-His332 would be more involved in S3 than in S2. This could be one element of the conformational changes put forward in the S2 to S3 transition.

AB - Oxygen evolution by Photosystem II (PSII) is catalyzed by a Mn 4Ca cluster. Thus far, from the crystallographic three-dimensional (3D) structures, seven amino acid residues have been identified as possible ligands of the Mn4Ca cluster. Among them, there is only one histidine, His332, which belongs to the D1 polypeptide. The relationships of the D1-His332 amino acid with kinetics and thermodynamic properties of the Mn 4Ca cluster in the S2- and S3-states of the catalytic cycle were investigated in purified PSII from Thermosynechococcus elongatus. This was done by examining site-directed D1-His332Gln and D1-His332Ser mutants by a variety of spectroscopic techniques such as time-resolved UV-visible absorption change spectroscopy, cw- and pulse-EPR, thermoluminescence, and measurement of substrate water exchange. Both mutants grew photo-autotrophically and active PSII could be purified. On the basis of the parameters assessed in this work, the D1-His332(Gln, Ser) mutations had no effect in the S2-state. Electron spin-echo envelope modulation (ESEEM) spectroscopy also showed that possible interactions between the nuclear spin of the nitrogen(s) of D1-His332 with the electronic spin S = 1/2 of the Mn4Ca cluster in the S2-state were not detectable and that the D1-His332Ser mutation did not affect the detected hyperfine couplings. In contrast, the following changes were observed in the S3-state of the D1-His332 mutants: (1) The redox potential of the S3/S2 couple was slightly increased by ≤20 meV, (2) The S3-EPR spectrum was slightly modified, (3) The D1-His332Gln mutation resulted in a ∼3 fold decrease of the slow (tightly bound) exchange rate and a ∼2 fold increase of the fast exchange rate of the water substrate molecules. All these results suggest that the D1-His332 would be more involved in S3 than in S2. This could be one element of the conformational changes put forward in the S2 to S3 transition.

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U2 - 10.1021/bi901067b

DO - 10.1021/bi901067b

M3 - Article

SN - 0006-2960

VL - 48

SP - 7856

EP - 7866

JO - Biochemistry

JF - Biochemistry

IS - 33

ER -

Evidence that D1-His332 in photosystem II from Thermosynechococcus elongatus interacts with the S3-state and not with the S2-state

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