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 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.

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); 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:https://doi.org/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:https://doi.org/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: https://doi.org/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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Works referencing / citing this record:

Evolution from S ₃ to S ₄ States of the Oxygen-Evolving Complex in Photosystem II Monitored by Quantum Mechanics/Molecular Mechanics (QM/MM) Dynamics
journal, June 2018

Narzi, Daniele; Capone, Matteo; Bovi, Daniele
Chemistry - A European Journal, Vol. 24, Issue 42
DOI: 10.1002/chem.201801709

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
journal, October 2018

Petrie, Simon; Stranger, Robert; Pace, Ron J.
ChemPhysChem, Vol. 19, Issue 23
DOI: 10.1002/cphc.201800686

Relative stability of the S2 isomers of the oxygen evolving complex of photosystem II
journal, April 2019

Kaur, Divya; Szejgis, Witold; Mao, Junjun
Photosynthesis Research, Vol. 141, Issue 3
DOI: 10.1007/s11120-019-00637-6

Thermodynamics of the S ₂ -to-S ₃ state transition of the oxygen-evolving complex of photosystem II
journal, January 2019

Amin, Muhamed; Kaur, Divya; Yang, Ke R.
Physical Chemistry Chemical Physics, Vol. 21, Issue 37
DOI: 10.1039/c9cp02308a

Pivotal role of the redox-active tyrosine in driving the water splitting catalyzed by photosystem II
journal, January 2020

Nakamura, Shin; Capone, Matteo; Narzi, Daniele
Physical Chemistry Chemical Physics, Vol. 22, Issue 1
DOI: 10.1039/c9cp04605d

An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser
journal, October 2019

Suga, Michihiro; Akita, Fusamichi; Yamashita, Keitaro
Science, Vol. 366, Issue 6463
DOI: 10.1126/science.aax6998

Water Network Dynamics Next to the Oxygen-Evolving Complex of Photosystem II
journal, March 2019

Reiss, Krystle; Morzan, Uriel; Grigas, Alex
Inorganics, Vol. 7, Issue 3
DOI: 10.3390/inorganics7030039

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
journal, April 2019

Pantazis, Dimitrios A.
Inorganics, Vol. 7, Issue 4
DOI: 10.3390/inorganics7040055

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

Abstract

Citation Formats

Figures / Tables:

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Water Network Dynamics Next to the Oxygen-Evolving Complex of Photosystem II journal, March 2019

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