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Pulse EPR Spectroscopic Characterization of the S3 State of the Oxygen-Evolving Complex of Photosystem II Isolated from Synechocystis

Cite this: Biochemistry 2020, 59, 51, 4864–4872
Publication Date (Web):December 15, 2020
https://doi.org/10.1021/acs.biochem.0c00880
Copyright © 2020 American Chemical Society
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Abstract

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The S3 state is the last semi-stable state in the water splitting reaction that is catalyzed by the Mn4O5Ca cluster that makes up the oxygen-evolving complex (OEC) of photosystem II (PSII). Recent high-field/frequency (95 GHz) electron paramagnetic resonance (EPR) studies of PSII isolated from the thermophilic cyanobacterium Thermosynechococcus elongatus have found broadened signals induced by chemical modification of the S3 state. These signals are ascribed to an S3 form that contains a five-coordinate MnIV center bridged to a cuboidal MnIV3O4Ca unit. High-resolution X-ray free-electron laser studies of the S3 state have observed the OEC with all-octahedrally coordinated MnIV in what is described as an open cuboid-like cluster. No five-coordinate MnIV centers have been reported in these S3 state structures. Here, we report high-field/frequency (130 GHz) pulse EPR of the S3 state in Synechocystis sp. PCC 6803 PSII as isolated in the presence of glycerol. The S3 state of PSII from Synechocystis exhibits multiple broadened forms (≈69% of the total signal) similar to those seen in the chemically modified S3 centers from T. elongatus. Field-dependent ELDOR-detected nuclear magnetic resonance resolves two classes of 55Mn nuclear spin transitions: one class with small hyperfine couplings (|A| ≈ 1–7 MHz) and another with larger hyperfine couplings (|A| ≈ 100 MHz). These results are consistent with an all-MnIV4 open cubane structure of the S3 state and suggest that the broadened S3 signals arise from a perturbation of Mn4A and/or Mn3B, possibly induced by the presence of glycerol in the as-isolated Synechocystis PSII.

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The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.biochem.0c00880.

  • PSII sample preparation information and EPR characterization (PDF)

Accession Codes

D1 protein from Synechocystis sp. PCC 6803, UniProtKB P16033.

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Cited By


This article is cited by 11 publications.

  1. Richard J. Debus. Alteration of the O2-Producing Mn4Ca Cluster in Photosystem II by the Mutation of a Metal Ligand. Biochemistry 2021, 60 (51) , 3841-3855. https://doi.org/10.1021/acs.biochem.1c00504
  2. Thomas A. Corry, Patrick J. O’Malley. S3 State Models of Nature’s Water Oxidizing Complex: Analysis of Bonding and Magnetic Exchange Pathways, Assessment of Experimental Electron Paramagnetic Resonance Data, and Implications for the Water Oxidation Mechanism. The Journal of Physical Chemistry B 2021, 125 (36) , 10097-10107. https://doi.org/10.1021/acs.jpcb.1c04459
  3. Alain Boussac, Miwa Sugiura, Julien Sellés. Probing the proton release by Photosystem II in the S1 to S2 high-spin transition. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2022, 1863 (5) , 148546. https://doi.org/10.1016/j.bbabio.2022.148546
  4. Koichi Miyagawa, Mitsuo Shoji, Hiroshi Isobe, Takashi Kawakami, Takahito Nakajima, Kizashi Yamaguchi. Relative energies among S3 intermediates in the photosystem II revealed by DLPNO coupled cluster and hybrid DFT calculations. Possible pathways of water insertion in the S2 to S3 transition. Chemical Physics Letters 2022, 793 , 139439. https://doi.org/10.1016/j.cplett.2022.139439
  5. Joshua Telser. Paramagnetic resonance investigation of mono- and di-manganese-containing systems in biochemistry. 2022,,, 315-372. https://doi.org/10.1016/bs.mie.2022.02.005
  6. Maria Drosou, Dimitrios A. Pantazis. Redox Isomerism in the S 3 State of the Oxygen‐Evolving Complex Resolved by Coupled Cluster Theory. Chemistry – A European Journal 2021, 10 https://doi.org/10.1002/chem.202101567
  7. Heui Beom Lee, Angela A. Shiau, David A. Marchiori, Paul H. Oyala, Byung‐Kuk Yoo, Jens T. Kaiser, Douglas C. Rees, R. David Britt, Theodor Agapie. CaMn 3 IV O 4 Cubane Models of the Oxygen‐Evolving Complex: Spin Ground States S <9/2 and the Effect of Oxo Protonation. Angewandte Chemie 2021, 133 (32) , 17812-17820. https://doi.org/10.1002/ange.202105303
  8. Heui Beom Lee, Angela A. Shiau, David A. Marchiori, Paul H. Oyala, Byung‐Kuk Yoo, Jens T. Kaiser, Douglas C. Rees, R. David Britt, Theodor Agapie. CaMn 3 IV O 4 Cubane Models of the Oxygen‐Evolving Complex: Spin Ground States S <9/2 and the Effect of Oxo Protonation. Angewandte Chemie International Edition 2021, 114 https://doi.org/10.1002/anie.202105303
  9. Maria Drosou, Georgia Zahariou, Dimitrios A. Pantazis. Orientational Jahn–Teller Isomerism in the Dark‐Stable State of Nature's Water Oxidase. Angewandte Chemie 2021, 133 (24) , 13605-13611. https://doi.org/10.1002/ange.202103425
  10. Maria Drosou, Georgia Zahariou, Dimitrios A. Pantazis. Orientational Jahn–Teller Isomerism in the Dark‐Stable State of Nature's Water Oxidase. Angewandte Chemie International Edition 2021, 60 (24) , 13493-13499. https://doi.org/10.1002/anie.202103425
  11. Maylis Orio, Dimitrios A. Pantazis. Successes, challenges, and opportunities for quantum chemistry in understanding metalloenzymes for solar fuels research. Chemical Communications 2021, 57 (33) , 3952-3974. https://doi.org/10.1039/D1CC00705J

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