Ultrafast Dynamics of Nonequilibrium Electron Transfer in Photoinduced Redox Cycle: Solvent Mediation and Conformation Flexibility

Abstract

We report here our systematic characterization of a photoinduced electron-transfer (ET) redox cycle in a covalently linked donor-spacer-acceptor flexible system, consisting of N-acetyl-tryptophan methylester as electron donor and thymine as electron acceptor in three distinct solvents of water, acetonitrile and dioxane. With femtosecond resolution, we determined all the ET time scales, forward and backward, by following the complete reaction evolution from reactants, to intermediates and finally to products. Surprisingly, we observed two distinct ET dynamics in water, corresponding to a stacked configuration with ultrafast ET in 0.7 ps and back ET in 4.5 ps and a partially folded C-clamp conformation with ET in 322 ps but back ET in 17 ps. In acetonitrile and dioxane, only the C-clamp conformations were observed with ET in 470 and 1068 ps and back ET in 110 and 94 ps, respectively. These relatively slow ET dynamics in hundreds of picoseconds all showed significant conformation heterogeneity and followed a stretched decay behavior. With both forward and back ET rates determined, we derived solvent reorganization energies and coupling constants. Significantly, we found that solvent molecules intercalated in the cleft of the C-clamp structure mediate electron transfer with a tunneling parameter (β) of 1.0–1.4 Å−1 and the high-frequency vibration modes in the product(s) couple with the back ET process, leading to the ultrafast back ET dynamics in tens of picoseconds. These findings provide mechanistic insights of nonequilibrium ET dynamics modulated by conformation flexibility, mediated by unique solvent configuration, and accelerated by vibrational coupling.

Curl flux, coherence, and population landscape of molecular systems: Nonequilibrium quantum steady state, energy (charge) transport, and thermodynamics

“…The quantum transport in terms of many-body description for nanoscale systems and single molecules was also studied 15,34 . The unidirectional electron flow in the non-equilibrium ultrafast electron transfer 52 was observed in recent experiments of photoreduction dynamics of oxidized photolyase 53 .…”

Dynamics and Mechanism of UV-Damaged DNA Repair in Indole–Thymine Dimer Adduct: Molecular Origin of Low Repair Quantum Efficiency

“…The overall signal can be deconvoluted into two components, as shown in the inset of the lower panel in Figure 1B. As in our extensively studied NATME-T system, 31 is not stable and intends to break the C5-C5' bond (see Scheme 2) immediately. According to theoretical studies on CPD dimer repair [35][36][37][38][39][40][41][42] and experimental observation in photolyase, 12, 13 the C5-C5' bond breaking (k SP1 in Scheme 2) is nearly barrierless and ultrafast within 10 ps.…”

“…[11][12][13]32 Here, the solvation relaxation of three solvents are ultrafast within a few picoseconds, but their conformational dynamics occur on the similar time scales of their ET reactions, leading to a stretched behavior. 31 Using the stretched-exponential-decay function…”

“…Clearly, the stretching parameter β in water is smaller than those in ACN and DIO, indicating more heterogeneous fluctuations in water. 31 Knowing the lifetime of (k d -1 ) of NATME * , the forward ET times can be obtained by favorable. For example, in water the reduction potential of NATME + is +1.05 eV 33 vs. NHE and is -1.96 eV for T<>T. 21 Using 4.13 eV as the 0-0 transition energy, 34 we obtained the free energy (∆G 0 ) of the forward ET as -1.1 eV.…”

“…With the knowledge of absorption coefficients of NATME * and NATME + from deconvolution of NATME-T model compound, 31 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 10 by excited-state NATME * , indicating that the NATME + signal contributes only a small portion ( Fig. 2A).…”