Ultrafast Dynamics of Nonequilibrium Short-Range Electron Transfer in Semiquinone Flavodoxin

Yang, Jie; Zhang, Yifei; Lu, Yangyi; Wang, Limin; Lu, Fang; Zhong, Dongping

doi:10.1021/acs.jpclett.2c00057

Cited by 8 publications

(9 citation statements)

References 46 publications

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“…The slow medium modes that make the dynamical control of electron transfer possible become dynamically frozen on the fast reaction time scale. Calculations of rates require a self-consistent solution for the reaction dynamics and nonergodic free energy surface over which diffusional dynamics proceed to the resonance tunneling configuration. − A clear signature of nonergodic dynamic freezing is the reduction , in the reorganization energy for primary charge separation from the thermodynamic limit of ∼2.46 eV obtained by MD to the experimentally observed value of ∼0.35 eV.…”

Section: Discussionmentioning

confidence: 99%

Theory of Protein Charge Transfer: Electron Transfer between Tryptophan Residue and Active Site of Azurin

Sarhangi

Matyushov

2022

J. Phys. Chem. B

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One reaction step in the conductivity relay of azurin, electron transfer between the Cu-based active site and the tryptophan residue, is studied theoretically and by classical molecular dynamics simulations. Oxidation of tryptophan results in electrowetting of this residue. This structural change makes the free energy surfaces of electron transfer nonparabolic as described by the Qmodel of electron transfer. We analyze the medium dynamical effect on protein electron transfer produced by coupled Stokes-shift dynamics and the dynamics of the donor−acceptor distance modulating electron tunneling. The equilibrium donor−acceptor distance falls in the plateau region of the rate constant, where it is determined by the protein−water dynamics, and the probability of electron tunneling does not affect the rate. The crossover distance found here puts most intraprotein electron-transfer reactions under the umbrella of dynamical control. The crossover between the medium-controlled and tunneling-controlled kinetics is combined with the effect of the protein−water medium on the activation barrier to formulate principles of tunability of protein-based charge-transfer chains. The main principle in optimizing the activation barrier is the departure from the Gaussian-Gibbsian statistics of fluctuations promoting activated transitions. This is achieved either by incomplete (nonergodic) sampling, breaking the link between the Stokes-shift and variance reorganization energies, or through wetting-induced structural changes of the enzyme's active site.

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Section: Discussionmentioning

confidence: 99%

Theory of Protein Charge Transfer: Electron Transfer between Tryptophan Residue and Active Site of Azurin

Sarhangi

Matyushov

2022

J. Phys. Chem. B

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“…Electron transfer is an important process in biology 1,2 , catalysis [3][4][5] , and artificial photosynthesis 6,7 . The environment (e.g., a solvent) plays an important active role in this process, rather than being a passive spectator [8][9][10][11][12][13] , and recent advances with time-resolved techniques, including X-ray spectroscopy, have given new insight into how the nonequilibrium dynamics of the environment affects electron transfer [14][15][16][17][18][19][20][21][22][23] . For example, for transition metal complexes, solvation dynamics strongly modulate intramolecular electron transfer and localization, rather than just perturbing it 21 .…”

Section: Introductionmentioning

confidence: 99%

Solvent dynamics of aqueous halides before and after photoionization

Reidelbach

Schneeberger

Zöllner

et al. 2022

Preprint

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Electron transfer reactions can be strongly influenced by solvent dynamics. We study the photoionization of halides in water as a model system for such reactions. There are no internal nuclear degrees of freedom in the solute, allowing to uniquely identify the dynamics of the solvent. We simulate the equilibrium solvent dynamics for Cl$^-$, Br$^-$, I$^-$ and their respective neutral atoms in water, comparing quantum mechanical/molecular mechanical (QM/MM) and classical molecular dynamics (MD) methods. On the basis of the obtained configurations, we calculate the extended X-Ray fine structure (EXAFS) spectra rigorously based on the MD snapshots and compare in detail with other theoretical and experimental results available in the literature. We find our EXAFS spectra based on QM/MM MD simulations in good agreement with their experimental counterparts for the ions. Classical MD simulations for the ions lead to EXAFS spectra that agree equally well with the experiment when it comes to the oscillatory period of the signal, even though they differ from the QM/MM radial distribution functions extracted from the MD. The amplitude is, however, considerably overestimated. This suggests that to judge the reliability of theoretical simulation methods or to elucidate fine details of the atomistic dynamics of the solvent based on EXAFS spectra, the amplitude and not only the oscillatory period need to be considered. If simulations fail qualitatively, as does the classical MD for the aqueous halogen atoms, the resulting EXAFS will also be strongly affected in both oscillatory period and amplitude. The good reliability of QM/MM-based EXAFS simulations, together with clear qualitative differences in the EXAFS spectra found between halides and their atomic counterparts, suggests that a combined theory and experimental EXAFS approach is suitable for elucidating the nonequilibrium solvent dynamics in the photoionization of halides, and possibly also for electron transfer reactions in more complex systems.

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“…8 ns, likely faster for ″ in ″-CS1). Fast ET rates, short contacts, strong through-space coupling between aromatic side chains, and complex relaxation dynamics covering a broad temporal range make Re126W124W122Cu I similar to systems for which a nonequilibrium short-range ET mechanism ,− has been postulated, as in Trp-containing flavoproteins. ,− This model is applicable to ET coupled to environmental (solvent) relaxation dynamics occurring on a comparable time scale. Coupling with environmental fluctuations reduces the outer sphere reorganization energy λ o and the driving force but by different amounts. ,,, It accounts well for experimentally determined ultrafast rates and predicts stretched-exponential kinetics .…”

Section: Discussionmentioning

confidence: 98%

Tryptophan to Tryptophan Hole Hopping in an Azurin Construct

Melčák,

Šebesta,

Heyda

et al. 2023

J. Phys. Chem. B

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Electron transfer (ET) between neutral and cationic tryptophan residues in the azurin construct [Re I (H126)-(CO) 3 (dmp)](W124)(W122)Cu I (dmp = 4,7-Me 2 -1,10-phenanthroline) was investigated by Born−Oppenheimer quantummechanics/molecular mechanics/molecular dynamics (QM/ MM/MD) simulations. We focused on W124 •+ ← W122 ET, which is the middle step of the photochemical hole-hopping process *Re II (CO) 3 (dmp •− ) ← W124 ← W122 ← Cu I , where sequential hopping amounts to nearly 10,000-fold acceleration over single-step tunneling (ACS Cent. Sci. 2019, 5, 192−200). In accordance with experiments, UKS-DFT QM/MM/MD simulations identified forward and reverse steps of W124 •+ ↔ W122 ET equilibrium, as well as back ET Re I (CO) 3 (dmp •− ) → W124 •+ that restores *Re II (CO) 3 (dmp •− ). Strong electronic coupling between the two indoles (≥40 meV in the crossing region) makes the productive W124 •+ ← W122 ET adiabatic. Energies of the two redox states are driven to degeneracy by fluctuations of the electrostatic potential at the two indoles, mainly caused by water solvation, with contributions from the protein dynamics in the W122 vicinity. ET probability depends on the orientation of Re(CO) 3 (dmp) relative to W124 and its rotation diminishes the hopping yield. Comparison with hole hopping in natural systems reveals structural and dynamics factors that are important for designing efficient hole-hopping processes.

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Ultrafast Dynamics of Nonequilibrium Short-Range Electron Transfer in Semiquinone Flavodoxin

Cited by 8 publications

References 46 publications

Theory of Protein Charge Transfer: Electron Transfer between Tryptophan Residue and Active Site of Azurin

Theory of Protein Charge Transfer: Electron Transfer between Tryptophan Residue and Active Site of Azurin

Solvent dynamics of aqueous halides before and after photoionization

Tryptophan to Tryptophan Hole Hopping in an Azurin Construct

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