Unraveling quantum coherences mediating primary charge transfer processes in photosystem II reaction center.

Photosystem II (PSII) reaction center (RC) is a unique complex that is capable of efficiently separating electronic charges across the membrane. The primary energy- and charge-transfer (CT) processes occur on comparable ultrafast timescales, which makes it extremely challenging to understand the fundamental mechanism responsible for the near-unity quantum efficiency of the transfer. Here, we elucidate the role of quantum coherences in the ultrafast energy and CT in the PSII RC by performing two-dimensional (2D) electronic spectroscopy at the cryogenic temperature of 20 kelvin, which captures the distinct underlying quantum coherences. Specifically, we uncover the electronic and vibrational coherences along with their lifetimes during the primary ultrafast processes of energy and CT. We construct an excitonic model that provides evidence for coherent energy and CT at low temperature in the 2D electronic spectra. The principles could provide valuable guidelines for creating artificial photosystems with exploitation of system-bath coupling and control of coherences to optimize the photon conversion efficiency to specific functions.

Multitype Electronic Interactions in Precursor Solutions of Molecular Doped P3HT Polymer.

Spin-casting of molecularly doped polymer solution mixtures is one of the commonly used methods to obtain conductive organic semiconductor films. In spin-casted films, electronic interaction between the dopant and polymer is one of the crucial factors that dictates the doping efficiency. Here, we investigate excitonic couplings using ultrafast two-dimensional electronic spectroscopy to examine the different types of electronic interactions in ion pairs of the prototype F4TCNQ-doped P3HT polymer system in a precursor solution mixture for spin-casting. Off-diagonal peaks in the 2D spectra clearly establish the excitonic coupling between P3HT+ and F4TCNQ- ions in solution. The observed excitonic coupling is the direct manifestation of a Coulombic interaction between the ion pair. The excited-state lifetime of F4TCNQ- in ion pairs shows biexponential decay at 30 and 200 fs, which hints toward the presence of a heterogeneous population with different interaction strengths. To examine the nature of these different types of interactions in solution mixtures, we study the system using molecular dynamics simulations on a fully solvated model employing the generalized Amber force field. We retrieve three dominant interaction modes of F4TCNQ anions with P3HT: side chain, π-stack, and slipped stack. To quantify these interactions, we complement our studies with electronic structure calculations, which reveal the excitonic coupling strengths of ∼ 75 cm-1 for side chain, ∼ 150 cm-1 for π-π-stack, and ∼69 cm-1 for slipped stack. These various interaction modes provide information about the key geometries of the seed structures in precursor solution mixtures, which may determine the final structures in spin-casted films. The insights gained from our study may guide new strategies to control and ultimately tune Coulomb interactions in polymer-dopant solutions.

Transient chiral dynamics revealed by two-dimensional circular dichroism spectroscopy.

Chirality has been considered as one of the key factors in the evolution of life in nature. It is important to uncover how chiral potentials of molecular systems play vital role in fundamental photochemical processes. Here, we investigate the role of chirality in photoinduced energy transfer in a model dimeric system, where the monomers are excitonically coupled. To observe transient chiral dynamics and energy transfer, we employ circularly polarized laser pulses in two-dimensional electronic spectroscopy to construct the two-dimensional circular dichroism (2DCD) spectral maps. Tracking time-resolved peak magnitudes in 2DCD spectra allows one to identify chirality induced population dynamics. The dynamics of energy transfer is revealed by the time-resolved kinetics of cross peaks. However, the differential signal of 2DCD spectra shows the magnitude of cross peaks is dramatically reduced at initial waiting time, which indicates the weak chiral interactions between two monomers. The downhill energy transfer is resolved by presenting a strong magnitude of cross peak in 2DCD spectra after long waiting time. The chiral contribution towards coherent and incoherent energy-transfer pathways in the model dimer system is further examined via control of excitonic couplings between two monomers. Applications are made to study the energy-transfer process in the Fenna-Matthews-Olson complex. Our work uncovers the potential of 2DCD spectroscopy to resolve the chiral-induced interactions and population transfers in excitonically coupled systems.

Quantum coherent energy transport in the Fenna-Matthews-Olson complex at low temperature.

In the primary step of natural light harvesting, the solar photon energy is captured in a photoexcited electron-hole pair, or an exciton, in chlorophyll. Its conversion to chemical potential occurs in the special pair reaction center, which is reached by downhill ultrafast excited-state energy transport through a network of chromophores. Being inherently quantum, transport could in principle occur via a matter wave, with vast implications for efficiency. How long a matter wave remains coherent is determined by the intensity by which the exciton is disturbed by the noisy biological environment. The stronger this is, the stronger the electronic coupling between chromophores must be to overcome the fluctuations and phase shifts. The current consensus is that under physiological conditions, quantum coherence vanishes on the 10-fs time scale, rendering it irrelevant for the observed picosecond transfer. Yet, at low-enough temperature, quantum coherence should in principle be present. Here, we reveal the onset of longer-lived electronic coherence at extremely low temperatures of ∼20 K. Using two-dimensional electronic spectroscopy, we determine the exciton coherence times in the Fenna-Matthew-Olson complex over an extensive temperature range. At 20 K, coherence persists out to 200 fs (close to the antenna) and marginally up to 500 fs at the reaction center. It decays markedly faster with modest increases in temperature to become irrelevant above 150 K. At low temperature, the fragile electronic coherence can be separated from the robust vibrational coherence, using a rigorous theoretical analysis. We believe that by this generic principle, light harvesting becomes robust against otherwise fragile quantum effects.

Ultrafast photoinduced dynamics of a donor-([Formula: see text])bridge-acceptor based merocyanine dye.

Merocyanine dyes are of great interest amongst researchers due to their nonlinear optical (NLO) properties and solvatochromism. Molecular structure of these dyes constitutes conjugated pathway between the donor and acceptor substituents, with lowest energy transition of [Formula: see text]-[Formula: see text]* character. To rationalize the design of these dyes and deduce structure-property relationship, it is eminent to unravel the excited state dynamics in these complex molecular structures in different solvents. Here we have studied excited state dynamics of a merocyanine dye known as HB194, which has shown commendable efficiency in small molecule based bulk heterojuction solar cells. We have employed femtosecond transient absorption in combination with the quantum chemistry calculations to unravel the solvent dependent charge transfer dynamics of HB194. The excited state decays of the HB194 in different solvents show multi-exponential components. The analysis of the time-resolved data reveals that the polar solvents induce conformationally relaxed intramolecular charge transfer state. In non-polar solvent cyclohexane, only solvent-stabilized ICT state is observed. Additionally, we observe an anomalously red-shifted emission in ethylene glycol centred at [Formula: see text] 750 nm. Our computational calculations suggest the presence of molecular dimers resulting into observed red-shifted emission band. Our work therefore underscores the importance of gathering molecular-level insight into the system-bath interactions for designing next generation merocynanine-based solvatochromic dyes.

Torsionally broken symmetry assists infrared excitation of biomimetic charge-coupled nuclear motions in the electronic ground state.

The concerted interplay between reactive nuclear and electronic motions in molecules actuates chemistry. Here, we demonstrate that out-of-plane torsional deformation and vibrational excitation of stretching motions in the electronic ground state modulate the charge-density distribution in a donor-bridge-acceptor molecule in solution. The vibrationally-induced change, visualised by transient absorption spectroscopy with a mid-infrared pump and a visible probe, is mechanistically resolved by ab initio molecular dynamics simulations. Mapping the potential energy landscape attributes the observed charge-coupled coherent nuclear motions to the population of the initial segment of a double-bond isomerization channel, also seen in biological molecules. Our results illustrate the pivotal role of pre-twisted molecular geometries in enhancing the transfer of vibrational energy to specific molecular modes, prior to thermal redistribution. This motivates the search for synthetic strategies towards achieving potentially new infrared-mediated chemistry.

Two-dimensional confinement for generating thin single crystals for applications in time-resolved electron diffraction and spectroscopy: an intramolecular proton transfer study.

Thin single organic crystals (≤1 µm) with large area (≥100 × 100 µm2) are desirable to explore photoinduced processes using ultrafast spectroscopy and electron-diffraction. Here, we present a general method based on spatial confinement to grow such crystals using the prototypical proton transfer system, 1,5-dihydroxyanthraquinone, as an example, and provide the protocol for optically characterizing structural dynamics to enable proper assignments using diffraction methods.

Fundamental Flaw in the Current Construction of the TiO2 Electron Transport Layer of Perovskite Solar Cells and Its Elimination.

The top-performing perovskite solar cells (efficiency > 20%) generally rely on the use of a nanocrystal TiO2 electron transport layer (ETL). However, the efficacies and stability of the current stereotypically prepared TiO2 ETLs employing commercially available TiO2 nanocrystal paste are far from their maximum values. As revealed herein, the long-hidden reason for this discrepancy is that acidic protons (∼0.11 wt %) always remain in TiO2 ETLs after high-temperature sintering due to the decomposition of the organic proton solvent (mostly alcohol). These protons readily lead to the formation of Ti-H species upon light irradiation, which act to block the electron transfer at the perovskite/TiO2 interface. Affront this challenge, we introduced a simple deprotonation protocol by adding a small amount of strong proton acceptors (sodium ethoxide or NaOH) into the common TiO2 nanocrystal paste precursor and replicated the high-temperature sintering process, which wiped out nearly all protons in TiO2 ETLs during the sintering process. The use of deprotonated TiO2 ETLs not only promotes the PCE of both MAPbI3-based and FA0.85MA0.15PbI2.55Br0.45-based devices over 20% but also significantly improves the long-term photostability of the target devices upon 1000 h of continuous operation.

Ultrafast Charge Transfer and Relaxation at a Donor-Acceptor Interface.

The efficiency of charge separation in organic photovoltaic materials is crucially determined by the underlying dynamics of the charge transfer (CT) excitons and their dissociation into free electrons and holes. To unravel the main principles of the underlying mechanism on a molecular level, we construct a toy model of electronically coupled donors interacting with a manifold of CT exciton states. In particular, we set up a ladder of CT site energies to model the exciton dissociation. To mimic the complexity of the exciton dynamics at the donor-acceptor interface, the electronic CT manifold is designed to include two vibrational modes that are vibronically coupled to the excitons. We examine the impact of the electronic and vibrational coherences and the structure of the vibronic manifold on the transfer efficiency and charge recombination. Optimal configurations of the vibronic CT manifold are revealed. In particular, the rate of charge recombination can be minimized when the transient dynamics are carefully explored. Such a toy model can be used as a guide for the design of organic materials for efficient photovoltaic devices.

Photoinduced Vibrations Drive Ultrafast Structural Distortion in Lead Halide Perovskite.

The success of organic-inorganic perovskites in optoelectronics is dictated by the complex interplay between various underlying microscopic phenomena. The structural dynamics of organic cations and the inorganic sublattice after photoexcitation are hypothesized to have a direct effect on the material properties, thereby affecting the overall device performance. Here, we use ultrafast heterodyne-detected two-dimensional (2D) electronic spectroscopy to reveal impulsively excited vibrational modes of methylammonium (MA) lead iodide perovskite, which drive the structural distortion after photoexcitation. Vibrational analysis of the measured data allows us to monitor the time-evolved librational motion of the MA cation along with the vibrational coherences of the inorganic sublattice. Wavelet analysis of the observed vibrational coherences reveals the coherent generation of the librational motion of the MA cation within ∼300 fs complemented with the coherent evolution of the inorganic skeletal motion. To rationalize this observation, we employed the configuration interaction singles (CIS), which support our experimental observations of the coherent generation of librational motions in the MA cation and highlight the importance of the anharmonic interaction between the MA cation and the inorganic sublattice. Moreover, our advanced theoretical calculations predict the transfer of the photoinduced vibrational coherence from the MA cation to the inorganic sublattice, leading to reorganization of the lattice to form a polaronic state with a long lifetime. Our study uncovers the interplay of the organic cation and inorganic sublattice during formation of the polaron, which may lead to novel design principles for the next generation of perovskite solar cell materials.

Intermolecular vibrations mediate ultrafast singlet fission.

Singlet fission is a spin-allowed exciton multiplication process in organic semiconductors that converts one spin-singlet exciton to two triplet excitons. It offers the potential to enhance solar energy conversion by circumventing the Shockley-Queisser limit on efficiency. We study the primary steps of singlet fission in a pentacene film by using a combination of TG and 2D electronic spectroscopy complemented by quantum chemical and nonadiabatic dynamics calculations. We show that the coherent vibrational dynamics induces the ultrafast transition from the singlet excited electronic state to the triplet-pair state via a degeneracy of potential energy surfaces, i.e., a multidimensional conical intersection. Significant vibronic coupling of the electronic wave packet to a few key intermolecular rocking modes in the low-frequency region connect the excited singlet and triplet-pair states. Along with high-frequency local vibrations acting as tuning modes, they open a new channel for the ultrafast exciton transfer through the resulting conical intersection.

Quantum biology revisited.

Photosynthesis is a highly optimized process from which valuable lessons can be learned about the operating principles in nature. Its primary steps involve energy transport operating near theoretical quantum limits in efficiency. Recently, extensive research was motivated by the hypothesis that nature used quantum coherences to direct energy transfer. This body of work, a cornerstone for the field of quantum biology, rests on the interpretation of small-amplitude oscillations in two-dimensional electronic spectra of photosynthetic complexes. This Review discusses recent work reexamining these claims and demonstrates that interexciton coherences are too short lived to have any functional significance in photosynthetic energy transfer. Instead, the observed long-lived coherences originate from impulsively excited vibrations, generally observed in femtosecond spectroscopy. These efforts, collectively, lead to a more detailed understanding of the quantum aspects of dissipation. Nature, rather than trying to avoid dissipation, exploits it via engineering of exciton-bath interaction to create efficient energy flow.

Intramolecular vibrations enhance the quantum efficiency of excitonic energy transfer.

We study the impact of underdamped intramolecular vibrational modes on the efficiency of the excitation energy transfer in a dimer in which each state is coupled to its own underdamped vibrational mode and, in addition, to a continuous background of environmental modes. For this, we use the numerically exact hierarchy equation of motion approach. We determine the quantum yield and the transfer time in dependence of the vibronic coupling strength, and in dependence of the damping of the incoherent background. Moreover, we tune the vibrational frequencies out of resonance with the excitonic energy gap. We show that the quantum yield is enhanced by up to 10% when the vibrational frequency of the donor is larger than at the acceptor. The vibronic energy eigenstates of the acceptor acquire then an increased density of states, which leads to a higher occupation probability of the acceptor in thermal equilibrium. We can conclude that an underdamped vibrational mode which is weakly coupled to the dimer fuels a faster transfer of excitation energy, illustrating that long-lived vibrations can, in principle, enhance energy transfer, without involving long-lived electronic coherence.

Does electronic coherence enhance anticorrelated pigment vibrations under realistic conditions?

The light-harvesting efficiency of a photoactive molecular complex is largely determined by the properties of its electronic quantum states. Those, in turn, are influenced by molecular vibrational states of the nuclear degrees of freedom. Here, we reexamine two recently formulated concepts that a coherent vibronic coupling between molecular states would either extend the electronic coherence lifetime or enhance the amplitude of the anticorrelated vibrational mode at longer times. For this, we study a vibronically coupled dimer and calculate the nonlinear two-dimensional (2D) electronic spectra that directly reveal electronic coherence. The time scale of electronic coherence is initially extracted by measuring the antidiagonal bandwidth of the central peak in the 2D spectrum at zero waiting time. Based on the residual analysis, we identify small-amplitude long-lived oscillations in the cross-peaks, which, however, are solely due to groundstate vibrational coherence, regardless of having resonant or off-resonant conditions. Our studies neither show an enhancement of the electronic quantum coherence nor an enhancement of the anticorrelated vibrational mode by the vibronic coupling under ambient conditions.

Ultrafast Energy Transfer in Excitonically Coupled Molecules Induced by a Nonlocal Peierls Phonon.

Molecular vibration can influence exciton transfer via either a local (intramolecular) Holstein or a nonlocal (intermolecular) Peierls mode. We show that a strong vibronic coupling to a nonlocal mode dramatically speeds up the transfer by opening an additional transfer channel. This Peierls channel is rooted in the formation of a conical intersection of the excitonic potential energy surfaces. For increasing Peierls coupling, the electronically coherent transfer for weak coupling turns into an incoherent transfer of a localized exciton through the intersection for strong coupling. The interpretation in terms of a conical intersection intuitively explains recent experiments of ultrafast energy transfer in photosynthetic and photovoltaic molecular systems.

Origin of poor doping efficiency in solution processed organic semiconductors.

Doping is an extremely important process where intentional insertion of impurities in semiconductors controls their electronic properties. In organic semiconductors, one of the convenient, but inefficient, ways of doping is the spin casting of a precursor mixture of components in solution, followed by solvent evaporation. Active control over this process holds the key to significant improvements over current poor doping efficiencies. Yet, an optimized control can only come from a detailed understanding of electronic interactions responsible for the low doping efficiencies. Here, we use two-dimensional nonlinear optical spectroscopy to examine these interactions in the course of the doping process by probing the solution mixture of doped organic semiconductors. A dopant accepts an electron from the semiconductor and the two ions form a duplex of interacting charges known as ion-pair complexes. Well-resolved off-diagonal peaks in the two-dimensional spectra clearly demonstrate the electronic connectivity among the ions in solution. This electronic interaction represents a well resolved electrostatically bound state, as opposed to a random distribution of ions. We developed a theoretical model to recover the experimental data, which reveals an unexpectedly strong electronic coupling of ∼250 cm-1 with an intermolecular distance of ∼4.5 Šbetween ions in solution, which is approximately the expected distance in processed films. The fact that this relationship persists from solution to the processed film gives direct evidence that Coulomb interactions are retained from the precursor solution to the processed films. This memory effect renders the charge carriers equally bound also in the film and, hence, results in poor doping efficiencies. This new insight will help pave the way towards rational tailoring of the electronic interactions to improve doping efficiencies in processed organic semiconductor thin films.

Primary Charge Separation in the Photosystem II Reaction Center Revealed by a Global Analysis of the Two-dimensional Electronic Spectra.

The transfer of electronic charge in the reaction center of Photosystem II is one of the key building blocks of the conversion of sunlight energy into chemical energy within the cascade of the photosynthetic reactions. Since the charge transfer dynamics is mixed with the energy transfer dynamics, an effective tool for the direct resolution of charge separation in the reaction center is still missing. Here, we use experimental two-dimensional optical photon echo spectroscopy in combination with the theoretical calculation to resolve its signature. A global fitting analysis allows us to clearly and directly identify a decay pathway associated to the primary charge separation. In particular, it can be distinguished from regular energy transfer and occurs on a time scale of 1.5 ps under ambient conditions. This technique provides a general tool to identify charge separation signatures from the energy transport in two-dimensional optical spectroscopy.

Tracking an electronic wave packet in the vicinity of a conical intersection.

This work treats the impact of vibrational coherence on the quantum efficiency of a dissipative electronic wave packet in the vicinity of a conical intersection by monitoring the time-dependent wave packet projection onto the tuning and the coupling mode. The vibrational coherence of the wave packet is tuned by varying the strength of the dissipative vibrational coupling of the tuning and the coupling modes to their thermal baths. We observe that the most coherent wave packet yields a quantum efficiency of 93%, but with a large transfer time constant. The quantum yield is dramatically decreased to 50% for a strongly damped incoherent wave packet, but the associated transfer time of the strongly localized wave packet is short. In addition, we find for the strongly damped wave packet that the transfer occurs via tunneling of the wave packet between the potential energy surfaces before the seam of the conical intersection is reached and a direct passage takes over. Our results provide direct evidence that vibrational coherence of the electronic wave packet is a decisive factor which determines the dynamical behavior of a wave packet in the vicinity of the conical intersection.

Nature does not rely on long-lived electronic quantum coherence for photosynthetic energy transfer.

During the first steps of photosynthesis, the energy of impinging solar photons is transformed into electronic excitation energy of the light-harvesting biomolecular complexes. The subsequent energy transfer to the reaction center is commonly rationalized in terms of excitons moving on a grid of biomolecular chromophores on typical timescales [Formula: see text]100 fs. Today's understanding of the energy transfer includes the fact that the excitons are delocalized over a few neighboring sites, but the role of quantum coherence is considered as irrelevant for the transfer dynamics because it typically decays within a few tens of femtoseconds. This orthodox picture of incoherent energy transfer between clusters of a few pigments sharing delocalized excitons has been challenged by ultrafast optical spectroscopy experiments with the Fenna-Matthews-Olson protein, in which interference oscillatory signals up to 1.5 ps were reported and interpreted as direct evidence of exceptionally long-lived electronic quantum coherence. Here, we show that the optical 2D photon echo spectra of this complex at ambient temperature in aqueous solution do not provide evidence of any long-lived electronic quantum coherence, but confirm the orthodox view of rapidly decaying electronic quantum coherence on a timescale of 60 fs. Our results can be considered as generic and give no hint that electronic quantum coherence plays any biofunctional role in real photoactive biomolecular complexes. Because in this structurally well-defined protein the distances between bacteriochlorophylls are comparable to those of other light-harvesting complexes, we anticipate that this finding is general and directly applies to even larger photoactive biomolecular complexes.

Two-dimensional photon echoes reveal non-Markovian energy transfer in an excitonic dimer.

We show that strong non-Markovian effects can be revealed by the steady-state two-dimensional (2D) photon echo spectra at asymptotic waiting times. For this, we use a simple dimer toy model that is strongly coupled to a harmonic bath with parameters typical for photoactive biomolecules. We calculate the 2D photon echo spectra employing both the numerically exact hierarchy equation of motion and the quasiadiabatic path integral approach and compare these results with approximate results from a time-nonlocal quantum master equation approach. While the latter correctly reproduces the exact population dynamics at long times, it fails at the same time to correctly describe the 2D photon echo spectra at long waiting times. The differences show that non-Markovian effects are much more important for the steady-state 2D photon echoes than for the equilibrium populations. Thus, accurate theoretical descriptions of the energy transfer dynamics in biomolecular complexes have to be based on numerically exact simulations of the environmental fluctuations when nonlinear response functions are analyzed.