Water Molecules Gating a Photoinduced One‐Electron Two‐Protons Transfer in a Tyrosine/Histidine (Tyr/His) Model of Photosystem II

Charalambidis, Georgios; Das, Shyamal; Trapali, Adelais; Quaranta, Annamaria; Orio, Maylis; Halime, Zakaria; Fertey, Pierre; Guillot, Régis; Coutsolelos, Athanassios G.; Leibl, Winfried; Aukauloo, Ally; Sircoglou, Marie

doi:10.1002/ange.201804498

Cited by 5 publications

(2 citation statements)

References 36 publications

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“…[18][19][20][21][22][23][24][25][26][27] In particular, benzimidazole phenol (BIP) constructs have been studied as models of the TyrZ-His190 pair. [28][29][30][31] Upon oxidation of the phenol, proton transfer to the benzimidazole occurs, generally perceived as an example of a concerted one-electron, one-proton transfer (EPT) process. 25 Electrochemical measurements show that the phenoxyl radical formed upon oxidation of BIP, 1 (Chart 1), which features an intramolecular H-bond between the phenol and the nitrogen at the 3-position of the imidazole, is thermodynamically capable of water oxidation near neutral pH.…”

Section: Introductionmentioning

confidence: 99%

Controlling Proton-Coupled Electron Transfer in Bioinspired Artificial Photosynthetic Relays

et al. 2018

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Bioinspired constructs consisting of benzimidazole-phenol moieties bearing N-phenylimines as proton-accepting substituents have been designed to mimic the H-bond network associated with the TyrZ-His190 redox relay in photosystem II. These compounds provide a platform to theoretically and experimentally explore and expand proton-coupled electron transfer (PCET) processes. The models feature H-bonds between the phenol and the nitrogen at the 3-position of the benzimidazole and between the 1H-benzimidazole proton and the imine nitrogen. Protonation of the benzimidazole and the imine can be unambiguously detected by infrared spectroelectrochemistry (IRSEC) upon oxidation of the phenol. DFT calculations and IRSEC results demonstrate that with sufficiently strong electron-donating groups at the para-position of the N-phenylimine group (e.g.,-OCH3 substitution), proton transfer to the imine is exergonic upon phenol oxidation, leading to a oneelectron, two-proton (E2PT) product with the imidazole acting as a proton relay. When transfer of the second proton is not sufficiently exergonic (e.g.,-CN substitution), a one-electron, one-proton transfer (EPT) product is dominant. Thus, the extent of proton translocation along the H-bond network, either ~1.6 Å or ~6.4 Å, can be controlled through imine substitution. Moreover, the H-bond strength between the benzimidazole NH and the imine nitrogen, which is a function of their relative pKa values, and the redox potential of the phenoxyl radical/phenol couple are linearly correlated with the Hammett constants of the substituents. In all cases, a high potential (~1 V vs SCE) is observed for the phenoxyl radical/phenol couple. Designing and tuning redox-coupled proton wires is important for understanding bioenergetics and developing novel artificial photosynthetic systems.

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Section: Introductionmentioning

confidence: 99%

Controlling Proton-Coupled Electron Transfer in Bioinspired Artificial Photosynthetic Relays

et al. 2018

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“…22−35 These studies, inspired by efforts to mimic the redox-active tyrosine residue (Y Z ) of PS II, highlight a range of mechanisms that are distinguished by single versus multisite PCET, electron-transfer driving force, solvent environment, the presence of hydrogen bond relays, and proximity of the proton donor and acceptor (reviewed by Pannwitz and Wenger 36 ). Yet, a protein matrix provides a heterogeneous environment for Trp and Tyr redox chemistry, and it is unclear whether lessons learned from model studies, which are often carried out in nonaqueous solvents (with exception 35 ), are fully applicable to these more complex systems. Moreover, most model systems are oxidative in nature and driven photochemically, whereas protein PCET can be both reductive and oxidative and initiated by a broad class of reactive ground-and excited-state species.…”

Section: ■ Introductionmentioning

confidence: 99%

Tuning Radical Relay Residues by Proton Management Rescues Protein Electron Hopping

2019

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Transient tyrosine and tryptophan radicals play key roles in the electron transfer (ET) reactions of photosystem (PS) II, ribonucleotide reductase (RNR), photolyase, and many other proteins. However, Tyr and Trp are not functionally interchangeable, and the factors controlling their reactivity are often unclear. Cytochrome c peroxidase (CcP) employs a Trp191 •+ radical to oxidize reduced cytochrome c (Cc). Although a Tyr191 replacement also forms a stable radical, it does not support rapid ET from Cc. Here we probe the redox properties of CcP Y191 by nonnatural amino acid substitution, altering the ET driving force and manipulating the protic environment of Y191. Higher potential fluorotyrosine residues increase ET rates marginally, but only addition of a hydrogen bond donor to Tyr191 • (via Leu232His or Glu) substantially alters activity by increasing the ET rate by nearly 30-fold. ESR and ESEEM spectroscopies, crystallography, and pH-dependent ET kinetics provide strong evidence for hydrogen bond formation to Y191 • by His232/Glu232. Rate measurements and rapid freeze quench ESR spectroscopy further reveal differences in radical propagation and Cc oxidation that support an increased Y191 • formal potential of ∼200 mV in the presence of E232. Hence, Y191 inactivity results from a potential drop owing to Y191 •+ deprotonation. Incorporation of a well-positioned base to accept and donate back a hydrogen bond upshifts the Tyr • potential into a range where it can effectively oxidize Cc. These findings have implications for the Y Z /Y D radicals of PS II, hole-hopping in RNR and cryptochrome, and engineering proteins for long-range ET reactions.

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Phthalocyanine as a Bioinspired Model for Chlorophyll f‐Containing Photosystem II Drives Photosynthesis into the Far‐Red Region

et al. 2021

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The textbook explanation that P680 pigments are the red limit to drive oxygenic photosynthesis must be reconsidered by the recent discovery that chlorophyll f (Chlf)‐containing Photosystem II (PSII) absorbing at 727 nm can drive water oxidation. Two different families of unsymmetrically substituted Zn phthalocyanines (Pc) absorbing in the 700–800 nm spectral window and containing a fused imidazole‐phenyl substituent or a fused imidazole‐hydroxyphenyl group have been synthetized and characterized as a bioinspired model of the Chlf/TyrosineZ/Histidine190 cofactors of PSII. Transient absorption studies in the presence of an electron acceptor and irradiating in the far‐red region evidenced an intramolecular electron transfer process. Visible and FT‐IR signatures indicate the formation of a hydrogen‐bonded phenoxyl radical in ZnPc II‐OH. This study sets the foundation for the utilization of a broader spectral window for multi‐electronic catalytic processes with one of the most robust and efficient dyes.

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Water Molecules Gating a Photoinduced One‐Electron Two‐Protons Transfer in a Tyrosine/Histidine (Tyr/His) Model of Photosystem II

Cited by 5 publications

References 36 publications

Controlling Proton-Coupled Electron Transfer in Bioinspired Artificial Photosynthetic Relays

Controlling Proton-Coupled Electron Transfer in Bioinspired Artificial Photosynthetic Relays

Tuning Radical Relay Residues by Proton Management Rescues Protein Electron Hopping

Phthalocyanine as a Bioinspired Model for Chlorophyll f‐Containing Photosystem II Drives Photosynthesis into the Far‐Red Region

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