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Title: Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions

Abstract

Photosystem II (PSII) performs the solar-driven oxidation of water used to fuel oxygenic photosynthesis. The active site of water oxidation is the oxygen-evolving complex (OEC), a Mn 4 CaO 5 cluster. PSII requires degradation of key subunits and reassembly of the OEC as frequently as every 20 to 40 min. The metals for the OEC are assembled within the PSII protein environment via a series of binding events and photochemically induced oxidation events, but the full mechanism is unknown. A role of proton release in this mechanism is suggested here by the observation that the yield of in vitro OEC photoassembly is higher in deuterated water, D 2 O, compared with H 2 O when chloride is limiting. In kinetic studies, OEC photoassembly shows a significant lag phase in H 2 O at limiting chloride concentrations with an apparent H/D solvent isotope effect of 0.14 ± 0.05. The growth phase of OEC photoassembly shows an H/D solvent isotope effect of 1.5 ± 0.2. We analyzed the protonation states of the OEC protein environment using classical Multiconformer Continuum Electrostatics. Combining experiments and simulations leads to a model in which protons are lost from amino acid that will serve as OEC ligandsmore » as metals are bound. Chloride and D 2 O increase the proton affinities of key amino acid residues. These residues tune the binding affinity of Mn 2+/3+ and facilitate the deprotonation of water to form a proposed μ-hydroxo bridged Mn 2+ Mn 3+ intermediate.« less

Authors:
ORCiD logo; ; ; ; ;
Publication Date:
Research Org.:
City Univ. of New York (CUNY), NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1562343
Alternate Identifier(s):
OSTI ID: 1610559
Grant/Contract Number:  
SC0001423; 822-HF17
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 38; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; photosystem II; assembly; inverse isotope effect; proton transfer; electrostatics

Citation Formats

Vinyard, David J., Badshah, Syed Lal, Riggio, M. Rita, Kaur, Divya, Fanguy, Annaliesa R., and Gunner, M. R. Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions. United States: N. p., 2019. Web. doi:10.1073/pnas.1910231116.
Vinyard, David J., Badshah, Syed Lal, Riggio, M. Rita, Kaur, Divya, Fanguy, Annaliesa R., & Gunner, M. R. Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions. United States. doi:10.1073/pnas.1910231116.
Vinyard, David J., Badshah, Syed Lal, Riggio, M. Rita, Kaur, Divya, Fanguy, Annaliesa R., and Gunner, M. R. Wed . "Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions". United States. doi:10.1073/pnas.1910231116.
@article{osti_1562343,
title = {Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions},
author = {Vinyard, David J. and Badshah, Syed Lal and Riggio, M. Rita and Kaur, Divya and Fanguy, Annaliesa R. and Gunner, M. R.},
abstractNote = {Photosystem II (PSII) performs the solar-driven oxidation of water used to fuel oxygenic photosynthesis. The active site of water oxidation is the oxygen-evolving complex (OEC), a Mn 4 CaO 5 cluster. PSII requires degradation of key subunits and reassembly of the OEC as frequently as every 20 to 40 min. The metals for the OEC are assembled within the PSII protein environment via a series of binding events and photochemically induced oxidation events, but the full mechanism is unknown. A role of proton release in this mechanism is suggested here by the observation that the yield of in vitro OEC photoassembly is higher in deuterated water, D 2 O, compared with H 2 O when chloride is limiting. In kinetic studies, OEC photoassembly shows a significant lag phase in H 2 O at limiting chloride concentrations with an apparent H/D solvent isotope effect of 0.14 ± 0.05. The growth phase of OEC photoassembly shows an H/D solvent isotope effect of 1.5 ± 0.2. We analyzed the protonation states of the OEC protein environment using classical Multiconformer Continuum Electrostatics. Combining experiments and simulations leads to a model in which protons are lost from amino acid that will serve as OEC ligands as metals are bound. Chloride and D 2 O increase the proton affinities of key amino acid residues. These residues tune the binding affinity of Mn 2+/3+ and facilitate the deprotonation of water to form a proposed μ-hydroxo bridged Mn 2+ Mn 3+ intermediate.},
doi = {10.1073/pnas.1910231116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 38,
volume = 116,
place = {United States},
year = {2019},
month = {9}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1910231116

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