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

doi:10.1021/acsenergylett.7b00750

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

Abstract

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 S ₁ state and the doubly flashed S ₃ 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.

Authors:

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

^[2];

^[2]

Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut 06520-8114, United States
Department of Chemistry, Yale University, New Haven, Connecticut 06520-8107, United States

Publication Date:: 2017-09-12

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

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Inst. of Health (NIH) (United States)

OSTI Identifier:: 1390663

Alternate Identifier(s):: OSTI ID: 1507570

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

Resource Type:: Published Article

Journal Name:: ACS Energy Letters

Additional Journal Information:: [Journal Name: ACS Energy Letters Journal Volume: 2 Journal Issue: 10]; Journal ID: ISSN 2380-8195

Publisher:: American Chemical Society (ACS)

Country of Publication:: United States

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats


                    Wang, Jimin, Askerka, Mikhail, Brudvig, Gary W., and Batista, Victor S. Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II.  United States: N. p., 2017. 
        Web.  doi:10.1021/acsenergylett.7b00750.

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                    Wang, Jimin, Askerka, Mikhail, Brudvig, Gary W., & Batista, Victor S. Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II.  United States.  doi:10.1021/acsenergylett.7b00750.

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                    Wang, Jimin, Askerka, Mikhail, Brudvig, Gary W., and Batista, Victor S. Tue .  
        "Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II".  United States.  doi:10.1021/acsenergylett.7b00750.

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@article{osti_1390663,

  title        = {Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II},

  author       = {Wang, Jimin and Askerka, Mikhail and Brudvig, Gary W. and Batista, Victor S.},

  abstractNote = {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.},

  doi          = {10.1021/acsenergylett.7b00750},

  journal      = {ACS Energy Letters},

  number       = [10],

  volume       = [2],

  place        = {United States},

  year         = {2017},

  month        = {9}

}

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DOI: 10.1021/acsenergylett.7b00750

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Cited by: 9 works

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Figure 1: Stereodiagram of superposition of the QM/MM S₁ (yellow, magenta, silver, red, and blue) and S₃ (salmon, green, dark magenta, pink, and blue) models, including six bidentate carboxylate ligands to highlight the moving parts to be expected in difference density features.

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