Concerted and Stepwise Proton-Coupled Electron Transfer for Tryptophan-Derivative Oxidation with Water as the Primary Proton Acceptor: Clarifying a Controversy

Nilsen-Moe, Astrid; Rosichini, Andrea; Glover, Starla D.; Hammarström, Leif

doi:10.1021/jacs.2c00371

Cited by 18 publications

(45 citation statements)

References 51 publications

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“…Interestingly, related pH-dependent behavior has recently been reported for photosystem II models . In these biomimetic studies, the PCET reaction involves deprotonation of an oxidized tryptophan with water as the proton acceptor with rate constants that increased as the solution pH was raised, rather than decreased as reported here.…”

Section: Discussionsupporting

confidence: 70%

“…Interestingly, related pH-dependent behavior has recently been reported for photosystem II models. 73 In these biomimetic studies, the PCET reaction involves deprotonation of an oxidized tryptophan with water as the proton acceptor with rate constants that increased as the solution pH was raised, rather than decreased as reported here. The difference in the direction of the rate constant change with pH is presumably due to a key detail of these reactions: in the prior biomimetic studies, the proton is transferred f rom the oxidized tryptophan to solution, whereas in the present work, the proton is transferred f rom the solution to the catalyst.…”

Section: ■ Discussionmentioning

confidence: 62%

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Reorganization Energies for Interfacial Proton-Coupled Electron Transfer to a Water Oxidation Catalyst

et al. 2022

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The reorganization energy (λ) for interfacial electron transfer (ET) and proton-coupled ET (PCET) from a conductive metal oxide (In 2 O 3 :Sn, ITO) to a surface-bound water oxidation catalyst was extracted from kinetic data measured as a function of the thermodynamic driving force. Visible light excitation resulted in rapid excited-state injection (k inj > 10 8 s −1 ) to the ITO, which photo-initiated the two interfacial reactions of interest. The rate constants for both reactions increased with the driving force, −ΔG°, to a saturating limit, k max , with rate constants consistently larger for ET than for PCET. Marcus−Gerischer analysis of the kinetic data provided the reorganization energy for interfacial PCET (0.90 ± 0.02 eV) and ET (0.40 ± 0.02 eV), respectively. The magnitude of k max for PCET was found to decrease with pH, behavior that was absent for ET. Both the decrease in k max and the larger reorganization energy for an unwanted competing PCET reaction from the ITO to the oxidized catalyst showcases a significant kinetic advantage for driving solar water oxidation at high pH. Computational analysis revealed a larger innersphere reorganization energy contribution for PCET than for ET arising from a more significant change in the Ru−O bond length for the PCET reaction. Extending the Marcus−Gerischer theory to PCET by including the excited electron−proton vibronic states and the proton donor−acceptor motion provided an apparent reorganization energy of 1.01 eV. This study demonstrates that the Marcus−Gerischer theory initially developed for ET can be reliably extended to PCET for quantifying and interpreting reorganization energies observed experimentally.

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Section: Discussionsupporting

confidence: 70%

Section: ■ Discussionmentioning

confidence: 62%

Reorganization Energies for Interfacial Proton-Coupled Electron Transfer to a Water Oxidation Catalyst

et al. 2022

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“…These findings should have far-reaching implications for biological ET reactions. For instance, the redox-active residues, especially Tyr and Trp, , are widely involved in biologically important proteins such as PSII, ,,− Ribonucleotide reductase (RNR), − LPMO, , and peroxidases. ,, In these proteins, the redox-active Tyr or Trp residues usually have H-bonding interactions with adjacent basic residues (e.g., Asp, Glu, His). In such cases, the adjacent base may mediate the ET/PCET process or stabilize the cation radical intermediate via H-bonding interactions. ,− Such a regulation would depend on the p K a of redox-active residues.…”

Section: Discussionmentioning

confidence: 99%

Understanding the Key Roles of pH Buffer in Accelerating Lignin Degradation by Lignin Peroxidase

Fang

Feng

Jiang

et al. 2023

JACS Au

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pH buffer plays versatile roles in both biology and chemistry. In this study, we unravel the critical role of pH buffer in accelerating degradation of the lignin substrate in lignin peroxidase (LiP) using QM/MM MD simulations and the nonadiabatic electron transfer (ET) and proton-coupled electron transfer (PCET) theories. As a key enzyme involved in lignin degradation, LiP accomplishes the oxidation of lignin via two consecutive ET reactions and the subsequent C−C cleavage of the lignin cation radical. The first one involves ET from Trp171 to the active species of Compound I, while the second one involves ET from the lignin substrate to the Trp171 radical. Differing from the common view that pH = 3 may enhance the oxidizing power of Cpd I via protonation of the protein environment, our study shows that the intrinsic electric fields have minor effects on the first ET step. Instead, our study shows that the pH buffer of tartaric acid plays key roles during the second ET step. Our study shows that the pH buffer of tartaric acid can form a strong H-bond with Glu250, which can prevent the proton transfer from the Trp171-H •+ cation radical to Glu250, thereby stabilizing the Trp171-H •+ cation radical for the lignin oxidation. In addition, the pH buffer of tartaric acid can enhance the oxidizing power of the Trp171-H •+ cation radical via both the protonation of the proximal Asp264 and the second-sphere H-bond with Glu250. Such synergistic effects of pH buffer facilitate the thermodynamics of the second ET step and reduce the overall barrier of lignin degradation by ∼4.3 kcal/mol, which corresponds to a rate acceleration of 10 3 -fold that agrees with experiments. These findings not only expand our understanding on pH-dependent redox reactions in both biology and chemistry but also provide valuable insights into tryptophanmediated biological ET reactions.

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“…These findings should have far-reaching implications for biological ET reactions. For instance, the redox-active residues, especially Tyr and Trp, 96,97 are widely involved in biologically important proteins such as PSII, 2,4,14,15,98,99 Ribonucleotide reductase (RNR), [100][101][102] LPMO, 103,104 and peroxidases. 102,105,106 In these proteins, the redox-active Tyr or Trp residues usually form H-bonding interactions with adjacent bases (e.g.…”

Section: Discussionmentioning

confidence: 99%

pH Accelerates the Long-Range Electron Transfer for Lignin Degradation via Second-Sphere H-Bonding Interactions

Fang

Feng

Jiang

et al. 2022

Preprint

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pH plays versatile roles in both biology and chemistry. For instance, pH can regulate the long-range electron transfer (ET) in many proteins. However, the mechanistic basis of many pH-dependent long-range ET processes remain unclear. In this study, we unravel the critical role of pH in accelerating the long-range ET in lignin peroxidase (LiP) using QM/MM MD simulations and the nonadiabatic ET and PCET theories. As a key enzyme involved in lignin degradation, LiP accomplishes the one-electron oxidation of lignin via two consecutive long-range ET reactions: the first one involves ET from Trp171 to the active species of Compound I, affording the Trp171 radical species, while the second one involves ET from the lignin substrate to the Trp171 radical, affording the lignin cation radical species. Our study demonstrates that pH can remarkably modulate the mechanism and kinetics of both ET reactions. Specifically, in the absence of the pH buffer of tartaric acid, our study shows that the first ET leads to a neutral Trp• radical, agreeing with the EPR experiments. Surprisingly, the addition of the tartaric acid stabilizes the Trp-H•+ cation radical via second-sphere H-bonding interactions and accelerates the ET rate for lignin oxidation by several orders of magnitude. These findings are consistent with the experimental information available, which not only expand our understanding on pH-dependent ET reactions in both biology and chemistry, but also provide valuable insights on tryptophan-mediated biological ET reactions.

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Concerted and Stepwise Proton-Coupled Electron Transfer for Tryptophan-Derivative Oxidation with Water as the Primary Proton Acceptor: Clarifying a Controversy

Cited by 18 publications

References 51 publications

Reorganization Energies for Interfacial Proton-Coupled Electron Transfer to a Water Oxidation Catalyst

Reorganization Energies for Interfacial Proton-Coupled Electron Transfer to a Water Oxidation Catalyst

Understanding the Key Roles of pH Buffer in Accelerating Lignin Degradation by Lignin Peroxidase

pH Accelerates the Long-Range Electron Transfer for Lignin Degradation via Second-Sphere H-Bonding Interactions

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