Photoinduced Proton-coupled Electron Transfer Research Articles

Redox Modulation of Flavin and Tyrosine Determines Photoinduced Proton-coupled Electron Transfer and Photoactivation of BLUF Photoreceptors

Photoinduced electron transfer in biological systems, especially in proteins, is a highly intriguing matter. Its mechanistic details cannot be addressed by structural data obtained by crystallography alone because this provides only static information on a given redox system. In combination with transient spectroscopy and site-directed manipulation of the protein, however, a dynamic molecular picture of the ET process may be obtained. In BLUF (blue light sensors using FAD) photoreceptors, proton-coupled electron transfer between a tyrosine and the flavin cofactor is the key reaction to switch from a dark-adapted to a light-adapted state, which corresponds to the biological signaling state. Particularly puzzling is the fact that, although the various naturally occurring BLUF domains show little difference in the amino acid composition of the flavin binding pocket, the reaction rates of the forward reaction differ quite largely from a few ps up to several hundred ps. In this study, we modified the redox potential of the flavin/tyrosine redox pair by site-directed mutagenesis close to the flavin C2 carbonyl and fluorination of the tyrosine, respectively. We provide information on how changes in the redox potential of either reaction partner significantly influence photoinduced proton-coupled electron transfer. The altered redox potentials allowed us furthermore to experimentally describe an excited state charge transfer intermediately prior to electron transfer in the BLUF photocycle. Additionally, we show that the electron transfer rate directly correlates with the quantum yield of signaling state formation.

Influence of Donor–Acceptor Distance Variation on Photoinduced Electron and Proton Transfer in Rhenium(I)–Phenol Dyads

A homologous series of four molecules in which a phenol unit is linked covalently to a rhenium(I) tricarbonyl diimine photooxidant via a variable number of p-xylene spacers (n = 0-3) was synthesized and investigated. The species with a single p-xylene spacer was structurally characterized to get some benchmark distances. Photoexcitation of the metal complex in the shortest dyad (n = 0) triggers release of the phenolic proton to the acetonitrile/water solvent mixture; a H/D kinetic isotope effect (KIE) of 2.0 ± 0.4 is associated with this process. Thus, the shortest dyad basically acts like a photoacid. The next two longer dyads (n = 1, 2) exhibit intramolecular photoinduced phenol-to-rhenium electron transfer in the rate-determining excited-state deactivation step, and there is no significant KIE in this case. For the dyad with n = 1, transient absorption spectroscopy provided evidence for release of the phenolic proton to the solvent upon oxidation of the phenol by intramolecular photoinduced electron transfer. Subsequent thermal charge recombination is associated with a H/D KIE of 3.6 ± 0.4 and therefore is likely to involve proton motion in the rate-determining reaction step. Thus, some of the longer dyads (n = 1, 2) exhibit photoinduced proton-coupled electron transfer (PCET), albeit in a stepwise (electron transfer followed by proton transfer) rather than concerted manner. Our study demonstrates that electronically strongly coupled donor-acceptor systems may exhibit significantly different photoinduced PCET chemistry than electronically weakly coupled donor-bridge-acceptor molecules.

Proton-Coupled Electron Transfer between 4-Cyanophenol and Photoexcited Rhenium(I) Complexes with Different Protonatable Sites

Two rhenium(I) tricarbonyl diimine complexes, one of them with a 2,2'-bipyrazine (bpz) and a pyridine (py) ligand in addition to the carbonyls ([Re(bpz)(CO)(3)(py)](+)), and one tricarbonyl complex with a 2,2'-bipyridine (bpy) and a 1,4-pyrazine (pz) ligand ([Re(bpy)(CO)(3)(pz)](+)) were synthesized, and their photochemistry with 4-cyanophenol in acetonitrile solution was explored. Metal-to-ligand charge transfer (MLCT) excitation occurs toward the protonatable bpz ligand in the [Re(bpz)(CO)(3)(py)](+) complex while in the [Re(bpy)(CO)(3)(pz)](+) complex the same type of excitation promotes an electron away from the protonatable pz ligand. This study aimed to explore how this difference in electronic excited-state structure affects the rates and the reaction mechanism for photoinduced proton-coupled electron transfer (PCET) between 4-cyanophenol and the two rhenium(I) complexes. Transient absorption spectroscopy provides clear evidence for PCET reaction products, and significant H/D kinetic isotope effects are observed in some of the luminescence quenching experiments. Concerted proton-electron transfer is likely to play an important role in both cases, but a reaction sequence of proton transfer and electron transfer steps cannot be fully excluded for the 4-cyanophenol/[Re(bpz)(CO)(3)(py)](+) reaction couple. Interestingly, the rate constants for bimolecular excited-state quenching are on the same order of magnitude for both rhenium(I) complexes.

Nonadiabatic Dynamics of Photoinduced Proton-Coupled Electron Transfer: Comparison of Explicit and Implicit Solvent Simulations

Theoretical approaches for simulating the ultrafast dynamics of photoinduced proton-coupled electron transfer (PCET) reactions in solution are developed and applied to a series of model systems. These processes are simulated by propagating nonadiabatic surface hopping trajectories on electron-proton vibronic surfaces that depend on the solute and solvent nuclear coordinates. The PCET system is represented by a four-state empirical valence bond model, and the solvent is treated either as explicit solvent molecules or as a dielectric continuum, in which case the solvent dynamics is described in terms of two collective solvent coordinates corresponding to the energy gaps associated with electron and proton transfer. The explicit solvent simulations reveal two distinct solvent relaxation time scales, where the faster time scale relaxation corresponds to librational motions of solvent molecules in the first solvation shell, and the slower time scale relaxation corresponds to the bulk solvent dielectric response. The charge transfer dynamics is strongly coupled to both the fast and slow time scale solvent dynamics. The dynamical multistate continuum theory is extended to include the effects of two solvent relaxation time scales, and the resulting coupled generalized Langevin equations depend on parameters that can be extracted from equilibrium molecular dynamics simulations. The implicit and explicit solvent approaches lead to qualitatively similar charge transfer and solvent dynamics for model PCET systems, suggesting that the implicit solvent treatment captures the essential elements of the nonequilibrium solvent dynamics for many systems. A combination of implicit and explicit solvent approaches will enable the investigation of photoinduced PCET processes in a variety of condensed phase systems.

A Pd(II)-hydroxyporphycene: synthesis, characterization, and photoinduced proton-coupled electron transfer

A Pd(II) complex, Pd(TPrPc-OH) (1, TPrPc-OH = 9-hydroxy-2,7,12,17-tetrapropylporphycenato dianion), has been synthesized and characterized. 1H NMR spectroscopy revealed that compound 1 exists as its enol form in solution. The H atom of the hydroxy group in 1 was exchanged with deuterium on addition of ethanol-d 6. UV–visible spectra showed a red shift of the Q band of 1 in THF compared with that of the acetoxy derivative Pd(TPrPc-OAc) (2, TPrPc-OAc = 9-acetoxy-2,7,12,17-tetrapropylporphycenato dianion). The pK a value of the hydroxy group in 1 was determined, by means of a UV–visible titration experiment, to be 10.56. A cyclic voltammogram of 1 in a mixture of THF and Britton–Robinson buffered aqueous solution revealed one-electron and one-proton coupled transfer in the oxidation process in the pH range from 2.7 to 10.5, which was identified by pH-varying experiments and the Pourbaix diagram. Transient absorption spectroscopy revealed that an electron-transfer reaction occurred from the triplet excited-state of 1 to 2,3,5,6-tetramethyl-1,4-benzoquinone (duroquinone, DQ) upon pulse laser irradiation at 532 nm. Such an intermolecular photoinduced electron-transfer reaction was not observed between the Ni analog, Ni(TPrPc-OH), and DQ. The reaction rate constant, k q, was indicative of a kinetic isotope effect with k q(H)/k q(D) = 1.7, supporting the belief that the exited-state electron transfer from 1 to DQ is accompanied by proton transfer.

Bis-semiquinone (bi-radical) formation by photoinduced proton coupled electron transfer in covalently linked catechol-quinone systems: Aviram’s hemiquinones revisited

The structure and reactivity of a covalently linked catechol-ortho-benzoquinone (hemiquinone) is studied by UV-Vis and IR absorption spectroscopy. Nanosecond transient absorption spectroscopy of the hemiquinone reveals the formation of bi-radical state consisting of two semiquinone units. It is a long-lived state resulting from proton coupled electron transfer (PCET).

Multidimensional treatment of stochastic solvent dynamics in photoinduced proton-coupled electron transfer processes: Sequential, concerted, and complex branching mechanisms

A theoretical approach for the multidimensional treatment of photoinduced proton-coupled electron transfer (PCET) processes in solution is presented. This methodology is based on the multistate continuum theory with an arbitrary number of diabatic electronic states representing the relevant charge distributions in a general PCET system. The active electrons and transferring proton(s) are treated quantum mechanically, and the electron-proton vibronic free energy surfaces are represented as functions of multiple scalar solvent coordinates corresponding to the single electron and proton transfer reactions involved in the PCET process. A dynamical formulation of the dielectric continuum theory is used to derive a set of coupled generalized Langevin equations of motion describing the time evolution of these collective solvent coordinates. The parameters in the Langevin equations depend on the solvent properties, such as the dielectric constants, relaxation time, and molecular moment of inertia, as well as the solute properties. The dynamics of selected intramolecular nuclear coordinates, such as the proton donor-acceptor distance or a torsional angle within the PCET complex, may also be included in this formulation. A surface hopping method in conjunction with the Langevin equations of motion is used to simulate the nonadiabatic dynamics on the multidimensional electron-proton vibronic free energy surfaces following photoexcitation. This theoretical treatment enables the description of both sequential and concerted mechanisms, as well as more complex processes involving a combination of these mechanisms. The application of this methodology to a series of model systems corresponding to collinear and orthogonal PCET illustrates fundamental aspects of these different mechanisms and elucidates the significance of proton vibrational relaxation and nonequilibrium solvent dynamics.

Correction to “Isotope Effects on the Nonequilibrium Dyanamics of Ultrafast Photoinduced Proton-Coupled Electron Transfer Reactions in Solution”

Correction to “Isotope Effects on the Nonequilibrium Dyanamics of Ultrafast Photoinduced Proton-Coupled Electron Transfer Reactions in Solution”

Current Theoretical Challenges in Proton-Coupled Electron Transfer: Electron–Proton Nonadiabaticity, Proton Relays, and Ultrafast Dynamics

Proton-coupled electron transfer (PCET) reactions play an important role in a wide range of biological and chemical processes. The motions of the electrons, transferring protons, solute nuclei, and solvent nuclei occur on a wide range of time scales and are often strongly coupled. As a result, the theoretical description of these processes requires a combination of quantum and classical methods. This Perspective discusses three of the current theoretical challenges in the field of PCET. The first challenge is the calculation of electron–proton nonadiabatic effects, which are significant for these reactions because the hydrogen tunneling is often faster than the electronic transition. The second challenge is the modeling of electron transfer coupled to proton transport along hydrogen-bonded networks. The third challenge is the simulation of the ultrafast dynamics of nonequilibrium photoinduced PCET reactions in solution. Insights provided by theoretical studies may assist in the design of more effective catalysts for energy conversion processes.

Isotope Effects on the Nonequilibrium Dynamics of Ultrafast Photoinduced Proton-Coupled Electron Transfer Reactions in Solution.

The hydrogen/deuterium isotope effects on the ultrafast dynamics of photoinduced proton-coupled electron transfer (PCET) are investigated with a recently developed nonadiabatic dynamics approach. An ensemble of surface hopping trajectories is propagated according to a Langevin equation on electron-proton vibronic free energy surfaces that depend on a collective solvent coordinate. The calculations illustrate that ultrafast PCET reactions could exhibit a significant normal isotope effect, where PCET is faster for hydrogen than deuterium, but could also exhibit a negligible isotope effect or even a slight inverse isotope effect. The isotope effect is very small or absent when highly excited electron-proton vibronic states dictate the nonadiabatic dynamics and increases with greater participation of lower vibronic states. Thus, although the presence of a significant isotope effect strongly suggests that proton motion is coupled to electron transfer, the absence of an isotope effect does not exclude the possibility that proton transfer accompanies electron transfer in ultrafast photoinduced charge transfer processes.

Ultrafast Interfacial Proton-Coupled Electron Transfer

Interfaces between metallic or semiconducting solids and protic solvent adsorbates or liquids represent one of the most important, and yet hardly explored material environments for proton coupled electron transfer (PCET) processes. PCET mediated dynamical phenomena driven by light, electron, and chemical potentials are central in energy transduction processes of vast economic and environmental importance including the photocatalytic splitting of H₂O, the photo and electrochemical reduction of CO₂, and the conversion of chemical to electrical energy in fuel cells. Experimental and theoretical investigations of the dynamical aspects of PCET at solid surfaces are particularly challenging because relatively localized charges within a solvent couple in the presence of strong interfacial potentials to delocalized states of electronic continua of semiconductor or metal electrodes. Moreover, the localized charges are never the bare protons and electrons that balance chemical equations, but rather are dressed particles with associated polarization clouds inhomogeneously distributed and comprised variously of free electrons, lattice ions, and solvent molecules. The polarization clouds screen the Coulomb potential on the medium specific time scales and impose energetic costs associated with transport through the inhomogeneous region of interfaces between the solid and molecular environments. We introduce some recent theoretical studies aimed at providing an atomisticmore » description on metal-protic solvent interface and modeling of simple processes such as the discharge of H⁺ at a metal interface. Because of the paucity of experimental research and embryonic stage of theory, our goal is to present some key theoretical concepts and early experimental efforts based primarily on a surface science approach to ultrafast electron induced dynamics. In order to introduce some key features of interfacial PCET in the strong and intermediate coupling regimes, we discuss specific examples of photoinduced dissociation of alkanes on metals and photoinduced PCET dynamics of methanol covered TiO₂ surfaces.« less

Role of Solvent Dynamics in Ultrafast Photoinduced Proton-Coupled Electron Transfer Reactions in Solution

A theoretical formulation for modeling photoinduced nonequilibrium proton-coupled electron transfer (PCET) reactions in solution is presented. In this formulation, the PCET system is described by donor and acceptor electron-proton vibronic free energy surfaces that depend on a single collective solvent coordinate. Dielectric continuum theory is used to obtain a generalized Langevin equation of motion for this collective solvent coordinate. The terms in this equation depend on the solvent properties, such as the dielectric constants, relaxation time, and molecular moment of inertia, as well as the solute properties characterizing the vibronic surfaces. The ultrafast dynamics following photoexcitation is simulated using a surface hopping method in conjunction with the Langevin equation of motion. This methodology is used to examine a series of model photoinduced PCET systems, where the initial nonequilibrium state is prepared by vertical photoexcitation from the ground electronic state to the donor electronic state. Analysis of the dynamical trajectories provides insight into the interplay between the solvent dynamics and the electron-proton transfer for these types of processes. In addition, these model studies illustrate how the coupling between the electron-proton transfer and the solvent dynamics can be tuned by altering the solute and solvent properties.

Dynamics of Photoinduced Proton-Coupled Electron Transfer at Molecule−Semiconductor Interfaces: A Reduced Density Matrix Approach

A theoretical model for describing the dynamics of photoinduced proton-coupled electron transfer (PCET) at molecule−semiconductor interfaces is presented. In this model, the electron is photoexcited to a molecular electronic state near the semiconductor surface, and the subsequent electron transfer to the conduction band of the semiconductor is coupled to a proton transfer reaction. The electron could be photoexcited from the ground to an excited electronic state within a dye molecule at the interface or from the defect band in the semiconductor to a molecular adsorbate layer. A model Hamiltonian is developed to describe this PCET process, and the equations of motion for the reduced density matrix elements in the basis of electron−proton vibronic states are derived. This formulation is used to calculate the time-dependent electronic and vibronic state populations for a series of model systems. These calculations provide insight into the hydrogen/deuterium isotope effect on the dynamics of the donor state population decay for ultrafast interfacial PCET. This isotope effect depends on the initial proton wavepacket and the relative time scales of the donor electronic state population decay and proton vibrational relaxation. The effects of the electronic coupling, temperature, and energy of the donor state on the population dynamics are also investigated for photoinduced interfacial electron transfer and PCET. The resulting theoretical predictions about the qualitative impact of altering system properties on the population decay time scales could be useful for designing catalysts that activate bonds containing hydrogen atoms.

Photoinduced homogeneous proton-coupled electron transfer: Model study of isotope effects on reaction dynamics

A model Hamiltonian for photoinduced homogeneous proton-coupled electron transfer reactions is presented, and the equations of motion for the reduced density matrix elements in an electron-proton vibronic basis are derived. This formalism enables a detailed analysis of the proton vibrational dynamics, as well as the dynamics of the electronic state populations, following photoexcitation. The application of this theory to model systems provides insight into the fundamental physical principles underlying these types of processes. The initial nonequilibrium state is prepared by vertical photoexcitation from the ground electronic state to a coherent vibrational mixture in the donor electronic state. This nonstationary state relaxes to the equilibrium distributions in the donor and acceptor electronic states via dynamical processes arising from nonadiabatic transitions between the donor and acceptor vibronic states concurrent with energy dissipation to the bath. During the initial stage, when the proton vibrational population in the donor state is distributed among higher vibrational states and the donor proton wavepacket is oscillating with large amplitude, the electronic state population dynamics exhibits virtually no hydrogen/deuterium isotope effect. After vibrational relaxation, when the proton vibrational population in the donor state becomes concentrated in the lower vibrational states and the donor proton wavepacket becomes more localized near the minimum of the donor potential, a significant hydrogen/deuterium isotope effect on the electronic state population dynamics is exhibited. These model system calculations lead to experimentally testable predictions about the qualitative behavior of these isotope effects.

Ru(TAP)2(dppz)]2+: a DNA intercalating complex, which luminesces strongly in water and undergoes photo-induced proton-coupled electron transfer with guanosine-5'-monophosphate.

The lowest excited state of [Ru(TAP)2(dppz)]2+ (TAP = 1,4,5,8-tetraazaphenanthrene, dppz = dipyrido[3,2-a:2',3'-c]phenazine) 1 is strongly luminescent, even in water, and very oxidizing. Therefore it is able to oxidise not only guanosine-5'-monophosphate (GMP), as demonstrated by laser flash photolysis, but also guanine-containing polynucleotides such as calf thymus DNA and [poly(dG-dC)]2. The luminescence quenching was found to be faster in H2O than in D2O, as is the back reaction, indicating that both processes probably proceed by proton-coupled electron transfer. These properties, that are controlled by the triplet MLCT state in which the charge has been transferred from the Ru to a TAP ligand, contrast with those of the well known [Ru(phen)2(dppz)]2+ 2.

Theoretical formulation for electron transfer coupled to multiple protons: Application to amidinium–carboxylate interfaces

This paper presents a theoretical formulation for electron transfer coupled to the motion of multiple protons. This theory is applied to proton-coupled electron transfer (PCET) through amidinium–carboxylate salt bridges, where the electron transfer reaction is coupled to the motion of two protons at the proton transfer interface. The rate for the donor–(amidinium–carboxylate)–acceptor system is found to be substantially slower than the rate for the switched interface donor–(carboxylate–amidinium)–acceptor system. This trend is consistent with experimental data for photoinduced PCET in analogous systems. The calculations indicate that this difference in rates is due mainly to the opposite dipole moments at the proton transfer interfaces for the two systems, leading to an endothermic reaction for the donor–(amidinium–carboxylate)–acceptor system and an exothermic reaction for the donor–(carboxylate–amidinium)–acceptor system. The deuterium kinetic isotope effects are found to be moderate (i.e., kH/kD<3) for both types of systems. These moderate kinetic isotope effects are due to the dominance of vibrationally excited product states, leading to significant overlap between the reactant and product proton vibrational wave functions.

Theoretical Study of Photoinduced Proton-Coupled Electron Transfer through Asymmetric Salt Bridges

The theoretical study in this paper is based on the experimental result that the rate of photoinduced electron transfer is 10 2 times slower through a donor-(amidinium-carboxylate)-acceptor salt bridge than through the corresponding switched interface donor-(carboxylate-amidinium)-acceptor complex (Kirby, J. P.; Roberts, J. A.; Nocera, D. G. J. Am. Chem. Soc. 1997, 119, 9230). This experimental result indicates that the proton-transfer interface plays an important role in these electron-transfer reactions. In this paper, a multistate continuum theory for proton-coupled electron transfer (PCET) is applied to analogues representing the chemical systems studied in these experiments. The solute is described with a multistate valence bond model, the solvent is represented as a dielectric continuum, and the active electrons and transferring proton(s) are treated quantum mechanically on equal footing. The application of this theory to these PCET systems provides adiabatic free energy surfaces that depend on two scalar solvent variables corresponding to the proton and electron transfer reactions. The theoretical analysis indicates that the experimentally observed difference in rates for the two chemical systems is due to differences in solute electrostatic properties, solvation energies, solvent reorganization energies, and electronic couplings. Moreover, this theoretical study provides insight into the underlying fundamental principles of PCET reactions.

Excited state dynamics with nonadiabatic transitions for model photoinduced proton-coupled electron transfer reactions

Photoinduced proton-coupled electron transfer is investigated for a minimal model consisting of three coupled degrees of freedom that represent an electron, a proton, and a collective solvent coordinate. Altering the parameters in this model generates a wide range of proton-coupled electron transfer (PCET) dynamics. Four different models are presented in this paper. Three of these models represent sequential mechanisms and one represents a concerted mechanism. The adiabatic potential energy curves as a function of solvent coordinate and the corresponding two-dimensional wave functions, which depend on both the proton and the electron coordinates, are calculated in order to study the possible mechanisms of photoinduced PCET. The surface hopping method “molecular dynamics with quantum transitions” (MDQT), which incorporates nonadiabatic transitions between adiabatic quantum states, is utilized to simulate the dynamics of photoinitiated PCET for two of these model systems. In this application of MDQT the proton and electron coordinates are treated quantum mechanically, and the solvent coordinate is treated classically. A relatively large number (e.g., 11) of mixed proton/electron adiabatic states are included in the MDQT simulations. The reaction is initiated on the electronically excited state, and many different dynamical pathways to lower energy stable states are observed. Nonadiabatic effects are shown to play an essential role in determining the rates and mechanisms of photoinduced PCET reactions. This paper differs from previous studies of PCET reactions in that it presents real-time nonadiabatic molecular dynamics simulations of model PCET reactions initiated on an electronically excited state.