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

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

doi:10.1021/acsenergylett.7b00750

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

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

Yale University

Research output: Contribution to journal › Article › peer-review

28 Citations (Scopus)

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.

Original language	English
Pages (from-to)	2299-2306
Number of pages	8
Journal	ACS Energy Letters
Volume	2
Issue number	10
DOIs	https://doi.org/10.1021/acsenergylett.7b00750
Publication status	Published - Oct 13 2017

ASJC Scopus subject areas

Chemistry (miscellaneous)
Renewable Energy, Sustainability and the Environment
Fuel Technology
Energy Engineering and Power Technology
Materials Chemistry

Access to Document

10.1021/acsenergylett.7b00750

Fingerprint Dive into the research topics of 'Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II'. Together they form a unique fingerprint.

Cite this

@article{0a87ecb73b4740fca0c4414c90e31a59,

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 {\AA} 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.",

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

note = "Funding Information: The authors acknowledge support by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences, and Biosciences, Photosynthetic Systems. Experimental work was funded by Grant DE-FG02-05ER15646 (G.W.B.), computational work was funded by Grant DESC0001423 (V.S.B), and crystallographic study was supported by National Institutes of Health Grant P01 GM022778 (J.W).",

year = "2017",

month = oct,

day = "13",

doi = "10.1021/acsenergylett.7b00750",

language = "English",

volume = "2",

pages = "2299--2306",

journal = "ACS Energy Letters",

issn = "2380-8195",

publisher = "American Chemical Society",

number = "10",

}

TY - JOUR

T1 - Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II

AU - Wang, Jimin

AU - Askerka, Mikhail

AU - Brudvig, Gary W.

AU - Batista, Victor S.

N1 - Funding Information: The authors acknowledge support by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences, and Biosciences, Photosynthetic Systems. Experimental work was funded by Grant DE-FG02-05ER15646 (G.W.B.), computational work was funded by Grant DESC0001423 (V.S.B), and crystallographic study was supported by National Institutes of Health Grant P01 GM022778 (J.W).

PY - 2017/10/13

Y1 - 2017/10/13

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85031286233&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85031286233&partnerID=8YFLogxK

U2 - 10.1021/acsenergylett.7b00750

DO - 10.1021/acsenergylett.7b00750

M3 - Article

AN - SCOPUS:85031286233

VL - 2

SP - 2299

EP - 2306

JO - ACS Energy Letters

JF - ACS Energy Letters

SN - 2380-8195

IS - 10

ER -