The open-cubane oxo–oxyl coupling mechanism dominates photosynthetic oxygen evolution: a comprehensive DFT investigation on O–O bond formation in the S<sub>4</sub>state

Guo, Yu; Li, Hui; He, Lanlan; Zhao, Dong‐Xia; Gong, Liutang; Yang, Zhong-Zhi

doi:10.1039/c7cp01617d

Cited by 32 publications

(48 citation statements)

References 146 publications

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“…The two S 2 isomers can lead to an open state for S 3 where the added substrate O is bound to the dangling Mn4 or a closed state where the substrate is on Mn1. The incomplete ligand shells of Mn1 and Mn4 in states below S 3 may deny a position for the second substrate water to bind before S 3 [42][43][44].…”

Section: Photosystem IImentioning

confidence: 99%

Tracing the Pathways of Waters and Protons in Photosystem II and Cytochrome c Oxidase

et al. 2019

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Photosystem II (PSII) uses water as the terminal electron donor, producing oxygen in the Mn4CaO5 oxygen evolving complex (OEC), while cytochrome c oxidase (CcO) reduces O2 to water in its heme–Cu binuclear center (BNC). Each protein is oriented in the membrane to add to the proton gradient. The OEC, which releases protons, is located near the P-side (positive, at low-pH) of the membrane. In contrast, the BNC is in the middle of CcO, so the protons needed for O2 reduction must be transferred from the N-side (negative, at high pH). In addition, CcO pumps protons from N- to P-side, coupled to the O2 reduction chemistry, to store additional energy. Thus, proton transfers are directly coupled to the OEC and BNC redox chemistry, as well as needed for CcO proton pumping. The simulations that study the changes in proton affinity of the redox active sites and the surrounding protein at different states of the reaction cycle, as well as the changes in hydration that modulate proton transfer paths, are described.

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Section: Photosystem IImentioning

confidence: 99%

Tracing the Pathways of Waters and Protons in Photosystem II and Cytochrome c Oxidase

et al. 2019

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“…With respect to dioxygen evolution, a long-held and currently popular view is that formation of the O-O bond occurs in the S 4 state or, more realistically, as part of a still unknown multistage S 3 -S 0 transition that has so far been explored only in various computational studies [35][36][37][38]. This means that O-O coupling would be initiated only after the final light-driven oxidation of the cluster, i.e., past the S 3 Y Z • state indicated in Figure 1d.…”

Section: Introductionmentioning

confidence: 99%

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

2019

Inorganics

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The catalytic cycle of the oxygen-evolving complex (OEC) of photosystem II (PSII) comprises five intermediate states Si (i = 0–4), from the most reduced S0 state to the most oxidized S4, which spontaneously evolves dioxygen. The precise geometric and electronic structure of the Si states, and hence the mechanism of O–O bond formation in the OEC, remain under investigation, particularly for the final steps of the catalytic cycle. Recent advances in protein crystallography based on X-ray free-electron lasers (XFELs) have produced new structural models for the S3 state, which indicate that two of the oxygen atoms of the inorganic Mn4CaO6 core of the OEC are in very close proximity. This has been interpreted as possible evidence for “early-onset” O–O bond formation in the S3 state, as opposed to the more widely accepted view that the O–O bond is formed in the final state of the cycle, S4. Peroxo or superoxo formation in S3 has received partial support from computational studies. Here, a brief overview is provided of spectroscopic information, recent crystallographic results, and computational models for the S3 state. Emphasis is placed on computational S3 models that involve O–O formation, which are discussed with respect to their agreement with structural information, experimental evidence from various spectroscopic studies, and substrate exchange kinetics. Despite seemingly better agreement with some of the available crystallographic interpretations for the S3 state, models that implicate early-onset O–O bond formation are hard to reconcile with the complete line of experimental evidence, especially with X-ray absorption, X-ray emission, and magnetic resonance spectroscopic observations. Specifically with respect to quantum chemical studies, the inconclusive energetics for the possible isoforms of S3 is an acute problem that is probably beyond the capabilities of standard density functional theory.

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“…更精确的单点能使用较高级别的基组 LANL2TZ(f) (Mn), LANL08 (Ca), cc-pvtz(-f) (C, H, O, N), 并应用 SMD 溶剂化模型 [38] (设置介电常数为 6.0 模拟弱极性的 PSII 蛋白质环境)和 DFT-D3 (BJ-damping) 色散作用校正 [39] . DFT 计算方法的所有细节均与前期工作 [33,40,41] 保持一致 . 因为本工作研究的水结合至 Mn 4 CaO 4 的过程不是单分子反应, 原则上除了零点能的贡献, 还应该考虑熵的效应, 所以能量统计时使用 Gibbs 自由能的形式(101 kPa, 298.15 K).…”

Section: 计算模型与方法unclassified

“…全部任务使用 Gaussian 09 [42] 完成, 执行于本实验室的 DELL 服务器 PowerEdge R630 (Linux-Fedora 21 操作系统). [41] ; 分析了开立方相比闭立方结构对于自由基耦合的异构体选择性的有利条件 [33]…”

Section: 计算模型与方法unclassified

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Possible Mechanisms of Water Binding to the Oxygen-Evolving Complex during the S₄-S₀ Transition: A Theoretical Investigation

郭宇¹,

刘瑜²,

戚娟娟³

et al. 2017

Acta Chim. Sinica

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It has been acknowledged that molecular oxygen produced in photosynthesis originates from water, rather than carbon dioxide. Dioxygen releases in the S 4-S 0 transition immediately prior to a new water binding to the oxygen-evolving complex, but hardly any investigation has been carried out on the binding mechanism up to date. Based on the open-cubane oxo-oxyl coupling mechanism in the S 4 state of photosynthetic oxygen evolution, in this study we propose three possible pathways of water binding to the oxygen-evolving complex Mn 4 CaO 4 during the S 4-S 0 transition, i.e. water binding to Ca trans to O5, water binding to Ca cis to O5, and water binding to Mn4 trans to O5. Broken-symmetry density functional theory (BS-DFT) calculations have demonstrated the thermodynamic feasibility for all these possible modes, without an overwhelming inclination for a certain manner. Besides, all these styles do not bring about any difference embodied in the experimental kinetic data on substrate water exchange in the S 1 , S 2 and S 3 states, for the basically same structures of the S 0 state derived from these different routes. Therefore, it is considered that the alternative mechanisms could coexist coordinately in the connecting stage between S-state cycles. Importantly, diverse forms of substrate selectivity are deduced according to different water binding ways, which exert obvious influences on the present and later S-cycles. In the long run, however, it can be seen that the two waters binding in the S 4-S 0 and S 2-S 3 periods together constitute the components of the released O 2. What matters is variation of the time to become substrates for different water binding modes during the S 4-S 0 transition, either in the current cycle or in the following cycles. Meanwhile, it is indicated that the dangler Mn4(III)/(IV) which possesses a five-coordinated pyramidal ligand field in both ' ' 0 3 S /S states, along with Ca(II) on which the carrousel rearrangement of water ligands can also occur, are essential structural elements of the S-state advancement and oxygen evolution. Thus, Mn4 and Ca may be in charge of water delivery to the active sites of Mn 4 CaO 5 from the nearby external water channels formed by crystal waters in hydrogen-bond interactions. On the whole, the geometric flexibility of the Mn cluster plays an important role in photosynthetic water oxidation. In the respects of water binding modes in the S 4-S 0 transition and corresponding substrate identifications for a specific S-cycle, we are looking forward to further confirmations or supplements from the experimental evidences of the targeted isotope labeling combined with mass spectrometry, infrared spectroscopy and site directed mutagenesis, etc. Our investigation may provide useful information and references for the mechanistic elucidations on photosynthetic water oxidation, especially in substrate water identifications. Keywords photosynthesis; oxygen-evolving complex; S 4-S 0 transition; water binding mechanism; water channel; broken

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The open-cubane oxo–oxyl coupling mechanism dominates photosynthetic oxygen evolution: a comprehensive DFT investigation on O–O bond formation in the S₄state

Cited by 32 publications

References 146 publications

Tracing the Pathways of Waters and Protons in Photosystem II and Cytochrome c Oxidase

Tracing the Pathways of Waters and Protons in Photosystem II and Cytochrome c Oxidase

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

Possible Mechanisms of Water Binding to the Oxygen-Evolving Complex during the S₄-S₀ Transition: A Theoretical Investigation

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The open-cubane oxo–oxyl coupling mechanism dominates photosynthetic oxygen evolution: a comprehensive DFT investigation on O–O bond formation in the S4state

Cited by 32 publications

References 146 publications

Tracing the Pathways of Waters and Protons in Photosystem II and Cytochrome c Oxidase

Tracing the Pathways of Waters and Protons in Photosystem II and Cytochrome c Oxidase

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

Possible Mechanisms of Water Binding to the Oxygen-Evolving Complex during the S4-S0 Transition: A Theoretical Investigation

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The open-cubane oxo–oxyl coupling mechanism dominates photosynthetic oxygen evolution: a comprehensive DFT investigation on O–O bond formation in the S₄state

Possible Mechanisms of Water Binding to the Oxygen-Evolving Complex during the S₄-S₀ Transition: A Theoretical Investigation