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Title: D1-S169A substitution of photosystem II reveals a novel S2-state structure

Abstract

In photosystem II (PSII), photosynthetic water oxidation occurs at the O2-evolving complex (OEC), a tetramanganese-calcium cluster that cycles through light-induced redox intermediates (S0 - S4) to produce oxygen from two substrate water molecules. The OEC is surrounded by a hydrogen-bonded network of amino-acid residues that plays a crucial role in proton transfer and substrate water delivery. Previously, we found that D1-S169 was crucial for water oxidation and its mutation to alanine perturbed the hydrogen-bonding network. In this study, we demonstrate that the activation energy for the S2 to S1 transition of D1-S169A PSII is higher than wild-type PSII with a ~1.7 - 2.7x slower rate of charge recombination with QA¯ relative to wild-type PSII. Arrhenius analysis of the decay kinetics shows an Ea of 5.87 ± 1.15 kcal mol–1 for decay back to the S1 state, compared to 0.80 ± 0.13 kcal mol–1 for the wild-type S2 state. In addition, we find that ammonia does not affect the S2-state EPR signal, indicating that ammonia does not bind to the Mn cluster in D1-S169A PSII. Lastly, a QM/MM analysis indicates that an additional water molecule binds to the Mn4 ion in place of an oxo ligand O5 in the S2 statemore » of D1-S169A PSII. The altered S2 state of D1-S169A PSII provides insight into the S2 → S3 state transition.« less

Authors:
; ; ; ; ; ;
Publication Date:
Research Org.:
Yale Univ., New Haven, CT (United States)
Sponsoring Org.:
USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1833470
Alternate Identifier(s):
OSTI ID: 1658414; OSTI ID: 1812293
Grant/Contract Number:  
FG02-05ER15646; SC0005291; SC0001423
Resource Type:
Published Article
Journal Name:
Biochimica et Biophysica Acta - Bioenergetics
Additional Journal Information:
Journal Name: Biochimica et Biophysica Acta - Bioenergetics Journal Volume: 1861 Journal Issue: 12; Journal ID: ISSN 0005-2728
Publisher:
Elsevier
Country of Publication:
Netherlands
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Cyanobacteria; Decay kinetics; Mutation; Oxygen evolution; Photosystem II; Structure

Citation Formats

Ghosh, Ipsita, Banerjee, Gourab, Reiss, Krystle, Kim, Christopher J., Debus, Richard J., Batista, Victor S., and Brudvig, Gary W. D1-S169A substitution of photosystem II reveals a novel S2-state structure. Netherlands: N. p., 2020. Web. doi:10.1016/j.bbabio.2020.148301.
Ghosh, Ipsita, Banerjee, Gourab, Reiss, Krystle, Kim, Christopher J., Debus, Richard J., Batista, Victor S., & Brudvig, Gary W. D1-S169A substitution of photosystem II reveals a novel S2-state structure. Netherlands. https://doi.org/10.1016/j.bbabio.2020.148301
Ghosh, Ipsita, Banerjee, Gourab, Reiss, Krystle, Kim, Christopher J., Debus, Richard J., Batista, Victor S., and Brudvig, Gary W. Tue . "D1-S169A substitution of photosystem II reveals a novel S2-state structure". Netherlands. https://doi.org/10.1016/j.bbabio.2020.148301.
@article{osti_1833470,
title = {D1-S169A substitution of photosystem II reveals a novel S2-state structure},
author = {Ghosh, Ipsita and Banerjee, Gourab and Reiss, Krystle and Kim, Christopher J. and Debus, Richard J. and Batista, Victor S. and Brudvig, Gary W.},
abstractNote = {In photosystem II (PSII), photosynthetic water oxidation occurs at the O2-evolving complex (OEC), a tetramanganese-calcium cluster that cycles through light-induced redox intermediates (S0 - S4) to produce oxygen from two substrate water molecules. The OEC is surrounded by a hydrogen-bonded network of amino-acid residues that plays a crucial role in proton transfer and substrate water delivery. Previously, we found that D1-S169 was crucial for water oxidation and its mutation to alanine perturbed the hydrogen-bonding network. In this study, we demonstrate that the activation energy for the S2 to S1 transition of D1-S169A PSII is higher than wild-type PSII with a ~1.7 - 2.7x slower rate of charge recombination with QA¯ relative to wild-type PSII. Arrhenius analysis of the decay kinetics shows an Ea of 5.87 ± 1.15 kcal mol–1 for decay back to the S1 state, compared to 0.80 ± 0.13 kcal mol–1 for the wild-type S2 state. In addition, we find that ammonia does not affect the S2-state EPR signal, indicating that ammonia does not bind to the Mn cluster in D1-S169A PSII. Lastly, a QM/MM analysis indicates that an additional water molecule binds to the Mn4 ion in place of an oxo ligand O5 in the S2 state of D1-S169A PSII. The altered S2 state of D1-S169A PSII provides insight into the S2 → S3 state transition.},
doi = {10.1016/j.bbabio.2020.148301},
journal = {Biochimica et Biophysica Acta - Bioenergetics},
number = 12,
volume = 1861,
place = {Netherlands},
year = {Tue Dec 01 00:00:00 EST 2020},
month = {Tue Dec 01 00:00:00 EST 2020}
}

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