Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II

Wang, Jimin; Askerka, Mikhail; Brudvig, Gary W.; Batista, Victor S.

doi:10.1021/acsenergylett.7b00750

Title: Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II

Journal Article · 09 September 2017 · ACS Energy Letters

DOI: https://doi.org/10.1021/acsenergylett.7b00750 · OSTI ID:1390663

Wang, Jimin ^[1]; Askerka, Mikhail ^[2];

^[2];

^[2]

Yale Univ., New Haven, CT (United States). Dept. of Molecular Biophysics and Biochemistry
Yale Univ., New Haven, CT (United States). Dept. of Chemistry

Photosystem II (PSII) oxidizes water to produce oxygen through a four-step photocatalytic cycle. Understanding PSII structure–function relations is important for the development of biomimetic photocatalytic systems. The quantum mechanics/molecular mechanics (QM/MM) analysis of substrate water binding to the oxygen-evolving complex (OEC) has suggested a rearrangement of water ligands in a carousel mechanism around a key Mn center. Here, we find that the most recently reported X-ray free-electron laser (XFEL) crystallographic data obtained for the dark-stable S₁ state and the doubly flashed S₃ state at 2.25 Å resolution support the carousel mechanism. The features in the XFEL data and QM/MM model-simulated difference Fourier maps suggest that water displacement may occur from the so-called “narrow” channel, resulting in binding of a new water molecule to the OEC, and thus provide new insights into the nature of rearrangements of water ligands along the catalytic cycle before O=O bond formation.

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Research Organization:: Yale Univ., New Haven, CT (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States)

Grant/Contract Number:: FG02-05ER15646; SC0001423; P01 GM022778; SC0001423, FG02- 05ER15646

OSTI ID:: 1390663

Alternate ID(s):: OSTI ID: 1507570

Journal Information:: ACS Energy Letters, Vol. 2, Issue 10; ISSN 2380-8195

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 52 works

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Structural and Oxidation State Changes of the Photosystem II Manganese Complex in Four Transitions of the Water Oxidation Cycle (S ₀ → S ₁ , S ₁ → S ₂ , S ₂ → S ₃ , and S _3,4 → S ₀ ) Characterized by X-ray Absorption Spectroscopy at 20 K and Room Temperature ^† Haumann, M.; Müller, C.; Liebisch, P. Biochemistry, Vol. 44, Issue 6 https://doi.org/10.1021/bi048697e	journal	February 2005
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Computational Insights on Crystal Structures of the Oxygen-Evolving Complex of Photosystem II with Either Ca ²⁺ or Ca ²⁺ Substituted by Sr ²⁺ Vogt, Leslie; Ertem, Mehmed Z.; Pal, Rhitankar Biochemistry, Vol. 54, Issue 3 https://doi.org/10.1021/bi5011706	journal	January 2015
Structural Changes in the Oxygen-Evolving Complex of Photosystem II Induced by the S ₁ to S ₂ Transition: A Combined XRD and QM/MM Study Askerka, Mikhail; Wang, Jimin; Brudvig, Gary W. Biochemistry, Vol. 53, Issue 44 https://doi.org/10.1021/bi5011915	journal	October 2014
Two Different Structures of the Oxygen-Evolving Complex in the Same Polypeptide Frameworks of Photosystem II Tanaka, Ayako; Fukushima, Yoshimasa; Kamiya, Nobuo Journal of the American Chemical Society, Vol. 139, Issue 5 https://doi.org/10.1021/jacs.6b09666	journal	January 2017
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren Nature, Vol. 473, Issue 7345 https://doi.org/10.1038/nature09913	journal	April 2011
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Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL Suga, Michihiro; Akita, Fusamichi; Sugahara, Michihiro Nature, Vol. 543, Issue 7643 https://doi.org/10.1038/nature21400	journal	February 2017
Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy Kern, Jan; Tran, Rosalie; Alonso-Mori, Roberto Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5371	journal	July 2014
Energetics of proton release on the first oxidation step in the water-oxidizing enzyme Saito, Keisuke; William Rutherford, A.; Ishikita, Hiroshi Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9488	journal	October 2015
Radiation Damage in XFEL: Case study from the oxygen-evolving complex of Photosystem II Amin, Muhamed; Badawi, Ashraf; Obayya, S. S. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep36492	journal	November 2016
Room temperature femtosecond X-ray diffraction of photosystem II microcrystals Kern, J.; Alonso-Mori, R.; Hellmich, J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 25, p. 9721-9726 https://doi.org/10.1073/pnas.1204598109	journal	June 2012
Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge ( -oxo) of the manganese tetramer Perez Navarro, M.; Ames, W. M.; Nilsson, H. Proceedings of the National Academy of Sciences, Vol. 110, Issue 39 https://doi.org/10.1073/pnas.1304334110	journal	September 2013
Simultaneous Femtosecond X-ray Spectroscopy and Diffraction of Photosystem II at Room Temperature Kern, J.; Alonso-Mori, R.; Tran, R. Science, Vol. 340, Issue 6131 https://doi.org/10.1126/science.1234273	journal	February 2013
The Structure of Photosystem II and the Mechanism of Water Oxidation in Photosynthesis Shen, Jian-Ren Annual Review of Plant Biology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120129	journal	April 2015

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An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser Suga, Michihiro; Akita, Fusamichi; Yamashita, Keitaro Science, Vol. 366, Issue 6463 https://doi.org/10.1126/science.aax6998	journal	October 2019
The S3 State of the Oxygen-Evolving Complex: Overview of Spectroscopy and XFEL Crystallography with a Critical Evaluation of Early-Onset Models for O–O Bond Formation Pantazis, Dimitrios A. Inorganics, Vol. 7, Issue 4 https://doi.org/10.3390/inorganics7040055	journal	April 2019
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Explaining the Different Geometries of the Water Oxidising Complex in the Nominal S ₃ State Crystal Structures of Photosystem II at 2.25 Å and 2.35 Å Petrie, Simon; Stranger, Robert; Pace, Ron J. ChemPhysChem, Vol. 19, Issue 23 https://doi.org/10.1002/cphc.201800686	journal	October 2018
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