The exchange of the fast substrate water in the S<sub>2</sub> state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

Lichtenberg, Casper de; Kim, Christopher J.; Chernev, Petko; Debus, Richard J.; Messinger, Johannes

doi:10.1039/d1sc02265b

Cited by 23 publications

(37 citation statements)

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“… 32 − 34 , 50 , 57 In addition to methodological differences, these studies modeled a Ca 2+ -bound W3 in the S 3 Y z state, 25 , 26 and an additional water molecule (W x ) bound to Mn1/Mn4. Recent experiments have further supported W3 as a substrate water molecule, 37 − 39 whereas previous experimental assignment supported W2. 27 − 30 We also note that rotation of the Mn4 ligands, as observed in the present ( Figure S3D ) as well as previous QM/MM simulations, 51 could exchange the identity of the water molecules.…”

Section: Discussionmentioning

confidence: 95%

“…Ugur et al ( 26 ) suggested that W3-deprotonation triggers the migration of this water molecule toward Mn1 (or to Mn4 in the closed cubane form), in a process that is favored by the oxidation of Tyr z , a finding that has recently gained indirect support from time-resolved X-ray free electron laser (XFEL) structures of PSII in the S 2 Y z → S 3 Y z transition 23 (but cf . also refs ( 35 ) and ( 36 )), Fourier transform infrared (FTIR) spectroscopic studies, 37 , 38 time-resolved membrane inlet mass spectrometric (TR-MIMS) experiments, 39 and other computational studies. 40 Importantly, water-exchange experiments revealed that all substrate water molecules are already bound in the S 2 Y z state 27 and that the (water/hydroxo/oxo) ligands observed in the refined X-ray structural models of this state 7 , 9 , 11 , 23 are thus likely substrate water candidates.…”

Section: Introductionmentioning

confidence: 99%

“… 13 Moreover, the discrepancy between the proposed substrate water candidates still remains unsolved. Although the involvement of W3 in the O 2 formation process 26 has recently gained further support, 9 , 11 , 22 , 39 it is currently unclear how Asp61, a residue that could be an important part in the proton pathway en route to the luminal aqueous phase, 13 , 46 functions as a proton acceptor for W3, as this residue is located >10 Å away from W3 on the other side of the Mn 4 O 5 Ca cluster ( Figure 1 C). Interestingly, in this context, recent time-resolved XFEL experiments 13 revealed conformational- and hydration changes along the Cl1 water/proton channel that is close to both Asp61 and Glu65 of subunit D1.…”

Section: Introductionmentioning

confidence: 99%

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Molecular Principles of Redox-Coupled Protonation Dynamics in Photosystem II

et al. 2022

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Photosystem II (PSII) catalyzes light-driven water oxidization, releasing O 2 into the atmosphere and transferring the electrons for the synthesis of biomass. However, despite decades of structural and functional studies, the water oxidation mechanism of PSII has remained puzzling and a major challenge for modern chemical research. Here, we show that PSII catalyzes redox-triggered proton transfer between its oxygen-evolving Mn 4 O 5 Ca cluster and a nearby cluster of conserved buried ion-pairs, which are connected to the bulk solvent via a proton pathway. By using multi-scale quantum and classical simulations, we find that oxidation of a redox-active Tyr z (Tyr161) lowers the reaction barrier for the water-mediated proton transfer from a Ca 2+ -bound water molecule (W3) to Asp61 via conformational changes in a nearby ion-pair (Asp61/Lys317). Deprotonation of this W3 substrate water triggers its migration toward Mn1 to a position identified in recent X-ray free-electron laser (XFEL) experiments [Ibrahim et al. Proc. Natl. Acad. Sci. USA 2020, 117, 12,624–12,635]. Further oxidation of the Mn 4 O 5 Ca cluster lowers the proton transfer barrier through the water ligand sphere of the Mn 4 O 5 Ca cluster to Asp61 via a similar ion-pair dissociation process, while the resulting Mn-bound oxo/oxyl species leads to O 2 formation by a radical coupling mechanism. The proposed redox-coupled protonation mechanism shows a striking resemblance to functional motifs in other enzymes involved in biological energy conversion, with an interplay between hydration changes, ion-pair dynamics, and electric fields that modulate the catalytic barriers.

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Section: Discussionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Molecular Principles of Redox-Coupled Protonation Dynamics in Photosystem II

et al. 2022

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“…During the S 2 -to-S 3 and S 3 -to-S 4 transitions, proton deprotonation precedes the oxidation of the Mn 4 Ca cluster. − The cluster is surrounded by an extensive network of H-bonds that merge into three well-defined pathways that lead to the thylakoid lumen. These pathways facilitate proton egress and/or substrate water access. ,− ,− …”

Section: Introductionmentioning

confidence: 99%

Alteration of the O₂-Producing Mn₄Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Debus

2021

Biochemistry

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The O 2 -evolving Mn 4 Ca cluster in photosystem II (PSII) is arranged as a distorted Mn 3 Ca cube that is linked to a fourth Mn ion (denoted as Mn4) by two oxo bridges. The Mn4 and Ca ions are bridged by residue D1-D170. This is also the only residue known to participate in the high-affinity Mn(II) site that participates in the light-driven assembly of the Mn 4 Ca cluster. In this study, we use Fourier transform infrared difference spectroscopy to characterize the impact of the D1-D170E mutation. On the basis of analyses of carboxylate and carbonyl stretching modes and the O−H stretching modes of hydrogen-bonded water molecules, we show that this mutation alters the extensive network of hydrogen bonds that surrounds the Mn 4 Ca cluster in the same manner as that of many other mutations. It also alters the equilibrium between conformers of the Mn 4 Ca cluster in the dark-stable S 1 state so that a high-spin form of the S 2 state is produced during the S 1 -to-S 2 transition instead of the low-spin form that gives rise to the S 2 state multiline electron paramagnetic resonance signal. The mutation may also change the coordination mode of the carboxylate group at position 170 to unidentate ligation of Mn4. This is the first mutation of a metal ligand in PSII that substantially impacts the spectroscopic signatures of the Mn 4 Ca cluster without substantially eliminating O 2 evolution. The results have significant implications for our understanding of the roles of alternate active/inactive conformers of the Mn 4 Ca cluster in the mechanism of O 2 formation.

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“…In photosystem II, the Mn 4 CaO 5 cluster is situated within a large protein complex in which the access of water is regulated by three channels. In addition, the water molecules near the Mn 4 CaO 5 cluster are arranged mainly along one face of the cluster, and they are highly ordered due to H-bonding networks that are supported by specific amino acids. − In case of molecular WOCs, the bulk water access may be limited by water/inert solvent mixtures (e.g., 3 M water in MeCN) or, more specifically, by embedding the catalyst in matrices such as MOFs, redox active polymers, or designed polypeptides/proteins …”

Section: Discussionmentioning

confidence: 99%

Water Oxidation by Pentapyridyl Base Metal Complexes? A Case Study

et al. 2022

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The design of molecular water oxidation catalysts (WOCs) requires a rational approach that considers the intermediate steps of the catalytic cycle, including water binding, deprotonation, storage of oxidizing equivalents, O–O bond formation, and O 2 release. We investigated several of these properties for a series of base metal complexes (M = Mn, Fe, Co, Ni) bearing two variants of a pentapyridyl ligand framework, of which some were reported previously to be active WOCs. We found that only [Fe(Py5 OMe )Cl] + (Py5 OMe = pyridine-2,6-diylbis[di-(pyridin-2-yl)methoxymethane]) showed an appreciable catalytic activity with a turnover number (TON) = 130 in light-driven experiments using the [Ru(bpy) 3 ] 2+ /S 2 O 8 2– system at pH 8.0, but that activity is demonstrated to arise from the rapid degradation in the buffered solution leading to the formation of catalytically active amorphous iron oxide/hydroxide (FeOOH), which subsequently lost the catalytic activity by forming more extensive and structured FeOOH species. The detailed analysis of the redox and water-binding properties employing electrochemistry, X-ray absorption spectroscopy (XAS), UV–vis spectroscopy, and density-functional theory (DFT) showed that all complexes were able to undergo the M III /M II oxidation, but none was able to yield a detectable amount of a M IV state in our potential window (up to +2 V vs SHE). This inability was traced to (i) the preference for binding Cl – or acetonitrile instead of water-derived species in the apical position, which excludes redox leveling via proton coupled electron transfer, and (ii) the lack of sigma donor ligands that would stabilize oxidation states beyond M III . On that basis, design features for next-generation molecular WOCs are suggested.

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The exchange of the fast substrate water in the S₂ state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

Abstract: The molecular oxygen we breathe is produced from water-derived oxygen species bound to the Mn4CaO5 cluster in photosystem II (PSII). Present research points to the central oxo-bridge O5 as the...

Cited by 23 publications

References 103 publications

Molecular Principles of Redox-Coupled Protonation Dynamics in Photosystem II

Molecular Principles of Redox-Coupled Protonation Dynamics in Photosystem II

Alteration of the O₂-Producing Mn₄Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Water Oxidation by Pentapyridyl Base Metal Complexes? A Case Study

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The exchange of the fast substrate water in the S2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

Abstract: The molecular oxygen we breathe is produced from water-derived oxygen species bound to the Mn4CaO5 cluster in photosystem II (PSII). Present research points to the central oxo-bridge O5 as the...

Cited by 23 publications

References 103 publications

Molecular Principles of Redox-Coupled Protonation Dynamics in Photosystem II

Molecular Principles of Redox-Coupled Protonation Dynamics in Photosystem II

Alteration of the O2-Producing Mn4Ca Cluster in Photosystem II by the Mutation of a Metal Ligand

Water Oxidation by Pentapyridyl Base Metal Complexes? A Case Study

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Product

Resources

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The exchange of the fast substrate water in the S₂ state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism

Alteration of the O₂-Producing Mn₄Ca Cluster in Photosystem II by the Mutation of a Metal Ligand