Development of bioinspired artificial photosynthetic systems

The specific objective of this review is to describe recent development of bioinspired artificial photosynthetic systems and their applications. First, multi-step electron-transfer systems composed of electron donor-acceptor ensembles are presented, mimicking functions of the photosynthetic reaction center. However, a significant amount of energy is lost during the multi-step electron-transfer processes. Then, as an alternative to conventional charge-separation functional molecular models based on multi-step long-range electron transfer within redox cascades, simple electron donor-acceptor dyads linked by covalent or non-covalent bonding have been developed to attain a long-lived and high-energy charge-separated state without significant loss of excitation energy. Such simple molecular dyads, capable of fast charge separation but extremely slow charge recombination, have significant advantages with regard to synthetic feasibility, providing a variety of applications including construction of organic solar cells and development of efficient photocatalytic systems for the solar energy conversion.     

Evidence against the hopping mechanism as an important electron transfer pathway for conformationally constrained oligopeptides

The rate constant of intramolecular electron transfer through oligopeptides based on the alpha-aminoisobutyric acid residue was determined as a function of the peptide length and found to depend weakly on the donor-acceptor separation. By measuring the electron-transfer activation energy and estimating the energy gap between donor and bridge, we were able to discard the electron hopping mechanism.     

Protein-water electrostatics and principles of bioenergetics

Despite its diversity, life universally relies on a simple basic mechanism of energy transfer in its energy chains-hopping electron transport between centers of electron localization on hydrated proteins and redox cofactors. Since many such hops connect the point of energy input with a catalytic site where energy is stored in chemical bonds, the question of energy losses in (nearly activationless) electron hops, i.e., energetic efficiency, becomes central for the understanding of the energetics of life. We show here that standard considerations based on rules of Gibbs thermodynamics are not sufficient, and the dynamics of the protein and the protein-water interface need to be involved. The rate of electronic transitions is primarily sensitive to the electrostatic potential at the center of electron localization. Numerical simulations show that the statistics of the electrostatic potential produced by hydration water are strongly non-Gaussian, with the breadth of the electrostatic noise far exceeding the expectations of the linear response. This phenomenon, which dramatically alters the energetic balance of a charge-transfer chain, is attributed to the formation of ferroelectric domains in the protein's hydration shell. These dynamically emerging and dissipating domains make the shell enveloping the protein highly polar, as gauged by the variance of the shell dipole which correlates with the variance of the protein dipole. The Stokes-shift dynamics of redox-active proteins are dominated by a slow component with the relaxation time of 100-500 ps. This slow relaxation mode is frozen on the time-scale of fast reactions, such as bacterial charge separation, resulting in a dramatically reduced reorganization free energy of fast electronic transitions. The electron transfer activation barrier becomes a function of the corresponding rate, self-consistently calculated from a non-ergodic version of the transition-state theory. The peculiar structure of the protein-water interface thus provides natural systems with two "non's"-non-Gaussian statistics and non-ergodic kinetics-to tune the efficiency of the redox energy transfer. Both act to reduce the amount of free energy released as heat in electronic transitions. These mechanisms are shown to increase the energetic efficiency of protein electron transfer by up to an order of magnitude compared to the "standard picture" based on canonical free energies and the linear response approximation. In other words, the protein-water tandem allows both the formation of a ferroelectric mesophase in the hydration shell and an efficient control of the energetics by manipulating the relaxation times.     

Electron-transfer state of 9-mesityl-10-methylacridinium ion with a much longer lifetime and higher energy than that of the natural photosynthetic reaction center

We have successfully achieved the electron-transfer (ET) state of 9-mesityl-10-methylacridinium ion, produced by a single step photoinduced electron transfer, which has a much longer lifetime (e.g., 2 h at 203 K) and higher energy (2.37 eV) than that of the natural system without loss of energy due to multistep electron-transfer processes.     

Fluorinated fullerenes: sources of donor-acceptor dyads with [18]trannulene acceptors for energy- and electron-transfer reactions

Fine-tuned control over the donor strength in a series of trannulenes-based donor-acceptor ensembles is used to alter the deactivation path of the photoexcited-state chromophore and to modulate the rates of intramolecular electron transfer. For the first time, a detailed analysis of emission spectra, time-dependent spectroscopic measurements, and electrochemistry prove spectroscopically and kinetically that trannulenes can serve, in a manner similar to C(60) and C(60) monoadducts, as both electron and also as energy acceptor in donor-acceptor ensembles, producing widely different electron-transfer regimes. This investigation also shows that the integration of trannulenes, as a versatile electron-acceptor building block, consistently produces charge recombination in the inverted Marcus region.     

Ab initio based calculations of electron-transfer rates in metalloproteins

A long-standing challenge in electron-transfer theory is to compute accurate rates of long-distance reactions in proteins. We describe an ab initio Hartree-Fock approach to compute electronic-coupling interactions and electron-transfer rates in proteins that allows the favorable comparison with experiment. The method includes the following key features; each is essential for reliable rate computations: (1) summing contributions over multiple tunneling pathways, (2) averaging couplings over thermally accessible protein conformations, (3) describing donor and acceptor electronic structure explicitly, including solvation effects, and averaging coupling over multiple energy-level crossings of the nearly degenerate donor-acceptor ligand-field states, and (4) eliminating basis set artifacts associated with diffuse basis functions. The strong dependence of coupling on donor-acceptor distance and on pathway interferences causes large variations of the computed electron-coupling values with protein geometry, and the strongest coupled conformers dominate the electron-transfer rate. As such, averaging over thermally accessible conformers of the protein and of the redox cofactors is essential. This approach was tested on six ruthenium-modified azurin derivatives using the high temperature nonadiabatic rate expression and compared with simpler pathways, average barrier, and semiempirical INDO models. Results of ab initio Hartree-Fock calculations with a split-valence basis set are in good agreement with the experimental rates. Predicted rates in the longer-distance derivatives are underestimated by 3-8-fold. This analysis indicates that the key ingredients needed for quantitatively reliable protein electron-transfer rate calculations are accessible.     

Photoinduced intramolecular electron transfer reactions within donor-acceptor linked compounds in solution and within donor-acceptor ion-pairs in crystal

Intramolecular electron transfer (ET) processes within donor-acceptor linked compounds in solution and donor-acceptor ion-pairs in crystal have been investigated by means of laser photolysis kinetic spectroscopy. An excited Ru(II)-moiety of donor-acceptor compounds undergoes intramolecular electron-transfer to either ruthenium(III) ion, rhodium(III) ion or a cobalt(III) ion, followed by back ET to regenerate the original reactant. An Arrhenius plot of the ET rate gave a straight line with an intercept (frequency factor) and a slope (activation energy) for the photoinduced ET and the back ET. Mixed-valence isomer states produced via photoinitiated ET rapidly decayed via back ET. A common and large frequency factor observed for Ru(II)-Rh(III) compounds is accounted for in terms of solvent-relaxation dynamics. For the back ET in the Ru(II)-Co(III) compounds, the frequency factors are reduced because of negative entropy change. ET within donor-acceptor ion-pair of Ru(bpy)₂³ and Co(CN)₃⁶ in crystal took place very rapidly compared with in water.     

Supramolecular electron transfer by anion binding

Anion binding has emerged as an attractive strategy to construct supramolecular electron donor-acceptor complexes. In recent years, the level of sophistication in the design of these systems has advanced to the point where it is possible to create ensembles that mimic key aspects of the photoinduced electron-transfer events operative in the photosynthetic reaction centre. Although anion binding is a reversible process, kinetic studies on anion binding and dissociation processes, as well as photoinduced electron-transfer and back electron-transfer reactions in supramolecular electron donor-acceptor complexes formed by anion binding, have revealed that photoinduced electron transfer and back electron transfer occur at time scales much faster than those associated with anion binding and dissociation. This difference in rates ensures that the linkage between electron donor and acceptor moieties is maintained over the course of most forward and back electron-transfer processes. A particular example of this principle is illustrated by electron-transfer ensembles based on tetrathiafulvalene calix[4]pyrroles (TTF-C4Ps). In these ensembles, the TTF-C4Ps act as donors, transferring electrons to various electron acceptors after anion binding. Competition with non-redox active substrates is also observed. Anion binding to the pyrrole amine groups of an oxoporphyrinogen unit within various supramolecular complexes formed with fullerenes also results in acceleration of the photoinduced electron-transfer process but deceleration of the back electron transfer; again, this is ascribed to favourable structural and electronic changes. Anion binding also plays a role in stabilizing supramolecular complexes between sulphonated tetraphenylporphyrin anions ([MTPPS](4-): M = H(2) and Zn) and a lithium ion encapsulated C(60) (Li(+)@C(60)); the resulting ensemble produces long-lived charge-separated states upon photoexcitation of the porphyrins.     

Geometry relaxation-induced large Stokes shift in red-emitting borondipyrromethenes (BODIPY) and applications in fluorescent thiol probes

2-Thienyl and 2,6-bisthienyl BODIPY derivatives (BS-SS and BS-DS) were prepared that show intense absorption (ε = 65000 M(-1) cm(-1) at 507 nm) and a large Stokes shift (96 nm) vs the small Stokes shift of typical BODIPY (<15 nm). Control compounds with a thienyl unit at the 8-position or phenyl substituents at the 2,6-positions were prepared (BS-1 and 9). BS-1 shows absorption/emission in the blue-shifted range and a small Stokes shift (12 nm). Compound 9 shows absorption in the red-shifted range, but the Stokes shift (<30 nm) is much smaller than that for BS-SS and BS-DS. DFT calculations propose the large Stokes shifts of BS-SS and BS-DS are due to the remarkable geometry relaxation upon photoexcitation and its substantial effect on the energy levels of molecular orbitals. For the dyes with small Stokes shifts, much smaller geometry relaxations were found. The fluorophores were used for fluorescent thiol probes, with 2,4-dinitrobenzenesulfonyl (DNBS) as the fluorescence switch. Both fluorescence OFF-ON and unprecedented ON-OFF transduction were observed, which are attributed to the different photoinduced intramolecular electron-transfer (PET) profile. All the photophysics were rationalized by DFT calculations based on the concept of "electronic states" instead of the very often used approximation of "molecular orbitals".     

Synthesis and photophysical properties of conjugated polymers with pendant 9,10-anthraquinone units

We have synthesized and investigated the photophysical properties of a series of electron-donor conjugated copolymers with pendant electron-acceptor units. The copolymers consist of diethynyl-1,4-phenylene, fluorene, or phenylene rings alternating with a phenylene unit bearing a pendant 9,10-anthraquinone moiety. The pendant donor-acceptor polymers were designed to have different optical pi-pi* band gaps, while the oxidation potential of the polymer backbone remains approximately constant in the series. The reduction potential of the donor-acceptor polymers is associated with the pendant acceptor units. This leads to the special situation that the electrochemical gap between oxidation and reduction potentials is constant, while the optical band gap decreases, going from PPP, via PPF, to PPE. This design is used to study the effect of the optical gap on the photoinduced electron-transfer reaction that occurs between the main chain electron donor and the pendant acceptor, while the same polymer architecture and energy of the charge separated state are maintained. Fluorescence and photoinduced absorption spectroscopy are used to study the electron transfer following photoexcitation in relation to solvent polarity and in thin solid films. For the fluorene-phenylene alternating copolymer, intramolecular photoinduced electron transfer occurs in the Marcus optimal region.     

Corrole-fullerene dyads: formation of long-lived charge-separated states in nonpolar solvents

The first example of covalently linked free-base corrole-fullerene dyads is reported. In the newly synthesized dyads, the free-energy calculations performed by employing the redox and singlet excited-state energy in both polar and nonpolar solvents suggested the possibility of electron transfer from the excited singlet state of corrole to the fullerene entity. Accordingly, steady-state and time-resolved emission studies revealed efficient fluorescence quenching of the corrole entity in the dyads. Further studies involving femtosecond laser flash photolysis and nanosecond transient absorption studies confirmed electron transfer to be the quenching mechanism, in which the electron-transfer product, the fullerene anion radical, was able to be spectrally characterized. The rate of charge separation, kCS, was found to be on the order of 10(10)-10(11) s(-1), suggesting an efficient photoinduced electron-transfer process. Interestingly, the rate of charge recombination, kCR, was slower by 5 orders of magnitude in nonpolar solvents, cyclohexane and toluene, resulting in a radical ion-pair lasting for several microseconds. Careful analysis of the kinetic and thermodynamic data using the Marcus approach revealed that this novel feature is due to appropriately positioning the energy level of the charge-separated state below the triplet states of either of the donor and acceptor entities in both polar and nonpolar solvents, a feature that was not evident in donor-acceptor dyads constructed using symmetric tetrapyrroles as electron donors.     

Charge-transfer emission of compact porphyrin-fullerene dyad analyzed by Marcus theory of electron-transfer

A porphyrin-fullerene dyad, which is characterized by a close proximity of the porphyrin donor and the fullerene acceptor, was found to undergo a photoinduced electron transfer both in solutions and in solid films. Near-infrared charge-transfer (CT) emission was observed and analyzed in frame of the semi-classical Marcus electron-transfer theory yielding values for the reaction free energy, -deltaG degrees = 1.75 eV, the internal reorganization energy, lambdav = 0.05 eV, and the donor-acceptor vibrational energy, hv(v) = 0.14 eV, both in solution and in solid film. The influence of the environment on the CT properties of the dyad is described by a single parameter, the outer-sphere reorganization energy, lambdas, which varies from 0.05 eV in non-polar solvents and films to 0.13 eV in solvents of moderate polarity. At low temperatures (T< 200 K), the CT emission consists of distinct bands shifted from each other by value hv(v). This is the first direct observation of the vibrational frequencies of a porphyrin-fullerene donor-acceptor system.     

Spectroscopic characterization of novel polycyclic aromatic polymers

A series of novel polyphenylenevinylene (PPV) derivative polymers were studied by absorption and photoluminescence spectroscopies. The effect of the sequential introduction of polycyclic aromatic ring substituents into the delocalized backbone was examined with relation to hypsochromatic and bathochromatic shifting. While the replacement of the phenyl units by naphthyl units results in a substantial hypsochromic shift of both the absorption and emission spectra, their subsequent substitution by anthryl units results in a bathochromic shift. The system is modeled according to, and is found to be consistent with, a previous study of donor-acceptor polyenes of varying length. The electronic structure of the backbone is found to be a balance between that of the high electron affinity polycyclic ring system and the contribution to conjugation across the linking vinyl unit. The model is adapted based on electron affinities of the constituent units, and a clear structure-property relationship for the absorption and emission properties of the system is elucidated. The Stokes shift is examined and is seen to be well-correlated with the vinyl contribution to the electron affinity total (EAtotal). The trends observed in the optical properties of the polymeric system are supported by Raman spectroscopy, whereby the spectral signature of the connecting vinyl bond is seen to soften in a fashion which is correlated with the modeled electron affinity parameters.     

Efficient charge separation in C60-based dyads: triazolino

Triazoline[4,5][60]fullerenes are strong electron acceptors that form with tetrathiafulvalene (TTF), a novel type of donor-acceptor dyad exhibiting efficient improved electron-transfer dynamics. In particular, a rapid photoinduced intramolecular electron transfer, forming a charge-separated state, is followed by a slow charge recombination to generate the fullerene triplet excited state in moderate quantum yields.     

Tetrathiafulvalene-based nanotweezers-noncovalent binding of carbon nanotubes in aqueous media with charge transfer implications

Electron donor-acceptor hybrids based on single wall carbon nanotubes (SWCNT) are one of the most promising functional structures that are currently developed in the emerging areas of energy conversion schemes and molecular electronics. As a suitable electron donor, π-extended tetrathiafulvalene (exTTF) stands out owing to its recognition of SWCNT through π-π stacking and electron donor-acceptor interactions. Herein, we explore the shape and electronic complementarity between different types of carbon nanotubes (CNT) and a tweezers-shaped molecule endowed with two exTTFs in water. The efficient electronic communication between semiconducting SWCNT/multiwall carbon nanotubes (MWCNT), on one hand, and the water-soluble exTTF nanotweezers 8, on the other hand, has been demonstrated in the ground and excited state by using steady-state as well as time-resolved spectroscopies, which were further complemented by microscopy. Importantly, appreciable electronic communication results in the electronic ground state having a shift of electron density, that is, from exTTFs to CNT, and in the electronic excited state having a full separation of electron density, that is oxidized exTTF and reduced CNT. Lifetimes in the range of several hundred picoseconds, which were observed for the corresponding electron transfer products upon light irradiation, tend to be appreciably longer in MWCNT/8 than in SWCNT/8.     

Difluoroboron β-diketonate dye with intense red/near-infrared fluorescence in solutions and solid states

We reported a difluoroboron β-diketonate dye that displays bright red/NIR fluorescence in both solutions and solid states.     

Proton-coupled electron transfer in soybean lipoxygenase

The proton-coupled electron transfer reaction catalyzed by soybean lipoxygenase-1 is studied with a multistate continuum theory that represents the transferring hydrogen nucleus as a quantum mechanical wave function. The inner-sphere reorganization energy of the iron cofactor is calculated with density functional theory, and the outer-sphere reorganization energy of the protein is calculated with the frequency-resolved cavity model for conformations obtained with docking simulations. Both classical and quantum mechanical treatments of the proton donor-acceptor vibrational motion are presented. The temperature dependence of the calculated rates and kinetic isotope effects is in agreement with the experimental data. The weak temperature dependence of the rates is due to the relatively small free energy barrier arising from a balance between the reorganization energy and the reaction free energy. The unusually high deuterium kinetic isotope effect of 81 is due to the small overlap of the reactant and product proton vibrational wave functions and the dominance of the lowest energy reactant and product vibronic states in the tunneling process. The temperature dependence of the kinetic isotope effect is strongly influenced by the proton donor-acceptor distance with the dominant contribution to the overall rate. This dominant proton donor-acceptor distance is significantly smaller than the equilibrium donor-acceptor distance and is determined by a balance between the larger coupling and the smaller Boltzmann probability as the distance decreases. Thus, the proton donor-acceptor vibrational motion plays a vital role in decreasing the dominant donor-acceptor distance relative to its equilibrium value to facilitate the proton-coupled electron transfer reaction.     

Water effects on electron transfer in azurin dimers

Recent experimental and theoretical analyses indicate that water molecules between or near redox partners can significantly affect their electron-transfer (ET) properties. Here, we study the effects of intervening water molecules on the electron self-exchange reaction of azurin (Az) by using a newly developed ab-initio method to calculate transfer integrals between molecular sites. We show that the insertion of water molecules in the gap between the copper active sites of Az dimers slows down the exponential decay of the ET rates with the copper-to-copper distance. Depending on the distance between the redox sites, water can enhance or suppress the electron-transfer kinetics. We show that this behavior can be ascribed to the simultaneous action of two competing effects: the electrostatic interaction of water with the protein subsystem and its ability to mediate ET coupling pathways.     

First-principles density-functional theory calculations of electron-transfer rates in azurin dimers

We have conceived and implemented a new method to calculate transfer integrals between molecular sites, which exploits few quantities derived from density-functional theory electronic structure computations and does not require the knowledge of the exact transition state coordinate. The method uses a complete multielectron scheme, thus including electronic relaxation effects. Moreover, it makes no use of empirical parameters. The computed electronic couplings can then be combined with estimates of the reorganization energy to evaluate electron-transfer rates that are measured in kinetic experiments: the latter are the basis to interpret electron-transfer mechanisms. We have applied our approach to the study of the electron self-exchange reaction of azurin, an electron-transfer protein belonging to the family of cupredoxins. The transfer integral estimates provided by the proposed method have been compared with those resulting from other computational techniques, from empirical models, and with available experimental data.