First-principles simulation of excitation energy transfer and transient absorption spectroscopy in the CP29 light-harvesting complex.

The dynamics of delocalized excitons in light-harvesting complexes (LHCs) can be investigated using different experimental techniques, and transient absorption (TA) spectroscopy is one of the most valuable methods for this purpose. A careful interpretation of TA spectra is essential for the clarification of excitation energy transfer (EET) processes occurring during light-harvesting. However, even in the simplest LHCs, a physical model is needed to interpret transient spectra as the number of EET processes occurring at the same time is very large to be disentangled from measurements alone. Physical EET models are commonly built by fittings of the microscopic exciton Hamiltonians and exciton-vibrational parameters, an approach that can lead to biases. Here, we present a first-principles strategy to simulate EET and transient absorption spectra in LHCs, combining molecular dynamics and accurate multiscale quantum chemical calculations to obtain an independent estimate of the excitonic structure of the complex. The microscopic parameters thus obtained are then used in EET simulations to obtain the population dynamics and the related spectroscopic signature. We apply this approach to the CP29 minor antenna complex of plants for which we follow the EET dynamics and transient spectra after excitation in the chlorophyll b region. Our calculations reproduce all the main features observed in the transient absorption spectra and provide independent insight on the excited-state dynamics of CP29. The approach presented here lays the groundwork for the accurate simulation of EET and unbiased interpretation of transient spectra in multichromophoric systems.

Fluorographene with impurities as a biomimetic light-harvesting medium.

We investigate the prospect of using a two-dimensional material, fluorographene, to mimic the light-harvesting function of natural photosynthetic antennas. We show by quantum chemical calculations that isles of graphene in a fluorographene sheet can act as quasi-molecules similar to natural pigments from which the structures similar in function to photosynthetic antennas can be built. The graphene isles retain enough identity so that they can be used as building blocks to which intuitive design principles of natural photosynthetic antennas can be applied. We examine the excited state properties, stability, and interactions of these building blocks. Constraints put on the antenna structure by the two-dimensionality of the material as well as the discrete nature of fluorographene sheet are studied. We construct a hypothetical energetic funnel out of two types of quasi-molecules to show how a limited number of building blocks can be arranged to bridge the energy gap and spatial separation in excitation energy transfer. Energy transfer rates for a wide range of the system-environment interaction strengths are predicted. We conclude that conditions for the near unity quantum efficiency of energy transfer are likely to be fulfilled in fluorographene with the controlled arrangement of quasi-molecules.

The atomistic modeling of light-harvesting complexes from the physical models to the computational protocol.

The function of light-harvesting complexes is determined by a complex network of dynamic interactions among all the different components: the aggregate of pigments, the protein, and the surrounding environment. Complete and reliable predictions on these types of composite systems can be only achieved with an atomistic description. In the last few decades, there have been important advances in the atomistic modeling of light-harvesting complexes. These advances have involved both the completeness of the physical models and the accuracy and effectiveness of the computational protocols. In this Perspective, we present an overview of the main theoretical and computational breakthroughs attained so far in the field, with particular focus on the important role played by the protein and its dynamics. We then discuss the open problems in their accurate modeling that still need to be addressed. To illustrate an effective computational workflow for the modeling of light harvesting complexes, we take as an example the plant antenna complex CP29 and its H111N mutant.

Exciton properties and optical spectra of light harvesting complex II from a fully atomistic description.

We present a fully atomistic simulation of linear optical spectra (absorption, fluorescence and circular dichroism) of the Light Harvesting Complex II (LHCII) trimer using a hybrid approach, which couples a quantum chemical description of the chlorophylls with a classical model for the protein and the external environment (membrane and water). The classical model uses a polarizable Molecular Mechanics force field, thus allowing mutual polarization effects in the calculations of the excitonic properties. The investigation is performed both on the crystal structure and on structures generated by a µs long classical molecular dynamics simulation of the complex within a solvated membrane. The results show that this integrated approach not only provides a good description of the excitonic properties and optical spectra without the need for additional refinements of the excitonic parameters, but it also allows an atomistic investigation of the relative importance of electronic, structural and environment effects in determining the optical spectra.

From Chalcogen Bonding to S-π Interactions in Hybrid Perovskite Photovoltaics.

The stability of hybrid organic-inorganic halide perovskite semiconductors remains a significant obstacle to their application in photovoltaics. To this end, the use of low-dimensional (LD) perovskites, which incorporate hydrophobic organic moieties, provides an effective strategy to improve their stability, yet often at the expense of their performance. To address this limitation, supramolecular engineering of noncovalent interactions between organic and inorganic components has shown potential by relying on hydrogen bonding and conventional van der Waals interactions. Here, the capacity to access novel LD perovskite structures that uniquely assemble through unorthodox S-mediated interactions is explored by incorporating benzothiadiazole-based moieties. The formation of S-mediated LD structures is demonstrated, including one-dimensional (1D) and layered two-dimensional (2D) perovskite phases assembled via chalcogen bonding and S-π interactions, through a combination of techniques, such as single crystal and thin film X-ray diffraction, as well as solid-state NMR spectroscopy, complemented by molecular dynamics simulations, density functional theory calculations, and optoelectronic characterization, revealing superior conductivities of S-mediated LD perovskites. The resulting materials are applied in n-i-p and p-i-n perovskite solar cells, demonstrating enhancements in performance and operational stability that reveal a versatile supramolecular strategy in photovoltaics.

Origin of Low-Lying Red States in the Lhca4 Light-Harvesting Complex of Photosystem I.

The antenna complexes of Photosystem I present low-lying states visible as red-shifted and broadened absorption and fluorescence bands. Among these, Lhca4 has the most evident features of these "red" states, with a fluorescence band shifted by more than 25 nm from typical LHC emission. This signal arises from a mixing of exciton and charge-transfer (CT) states within the excitonically coupled a603-a609 chlorophyll (Chl) dimer. Here we combine molecular dynamics, multiscale quantum chemical calculations, and spectral simulations to uncover the molecular mechanism for the formation and tuning of exciton-CT interactions in Lhca4. We show that the coupling between exciton and CT states is extremely sensitive to tiny variations in the Chl dimer arrangement, explaining both the red-shifted bands and the switch between conformations with blue and red emission observed in single-molecule spectroscopy. Finally, we show that mutating the axial ligand of a603 diminishes the exciton-CT coupling, removing any red-state fingerprint.

Isolating Pure Donor and Acceptor Signals by Polarization-Controlled Transient Absorption Spectroscopy.

The optical spectra of molecules are often highly congested, inhibiting definite assignment of features and dynamics. In this work, we demonstrate and apply a polarization-based strategy for the decomposition of time-resolved optical spectra to analyze the electronic structure and energy transfer in a molecular donor-acceptor (D-A) dyad. We choose a dyad with orthogonal transition dipole moments for D and A and high fluorescence quantum yield to show that polarization-controlled ultrafast transient absorption spectra can isolate the pure D and A parts of the total signal. This provides a strategy to greatly reduce spectral congestion in complex systems and thus allows for detailed studies of electronic structure and electronic energy transfer.

Excitonic Nature of Carotenoid-Phthalocyanine Dyads and Its Role in Transient Absorption Spectra.

Artificial carotenoid-tetrapyrrole dyads have been extensively used as model systems to understand the quenching mechanisms that occur in light-harvesting complexes during nonphotochemical quenching. In particular, dyads containing a carotenoid covalently linked to a zinc phthalocyanine have been studied by transient absorption spectroscopy, and the observed signals have been interpreted in terms of an excitonically coupled state involving the lowest excited states of the two fragments. If present, such excitonic delocalization would have significant implications on the mechanism of nonphotochemical quenching. Here, we use quantum chemical calculations to show that this delocalization is not needed to reproduce the transient absorption spectra. On the contrary, the observed signals can be explained through excitonic couplings in the higher-energy manifold of states. We also argue that the covalent linkage between the two fragments allows for electronic communications, which complicates the analysis of the spectra based on two independent but coupled moieties. These findings call for a more thorough reassessment of the photophysics in these dyads and its implications in the context of natural nonphotochemical quenching.

Structure of the stress-related LHCSR1 complex determined by an integrated computational strategy.

Light-harvesting complexes (LHCs) are pigment-protein complexes whose main function is to capture sunlight and transfer the energy to reaction centers of photosystems. In response to varying light conditions, LH complexes also play photoregulation and photoprotection roles. In algae and mosses, a sub-family of LHCs, light-harvesting complex stress-related (LHCSR), is responsible for photoprotective quenching. Despite their functional and evolutionary importance, no direct structural information on LHCSRs is available that can explain their unique properties. In this work, we propose a structural model of LHCSR1 from the moss P. patens, obtained through an integrated computational strategy that combines homology modeling, molecular dynamics, and multiscale quantum chemical calculations. The model is validated by reproducing the spectral properties of LHCSR1. Our model reveals the structural specificity of LHCSR1, as compared with the CP29 LH complex, and poses the basis for understanding photoprotective quenching in mosses.

Anharmonic Molecular Motion Drives Resonance Energy Transfer in peri-Arylene Dyads.

Spectral and dynamical properties of molecular donor-acceptor systems strongly depend on the steric arrangement of the constituents with exciton coupling J as a key control parameter. In the present work we study two peri-arylene based dyads with orthogonal and parallel transition dipoles for donor and acceptor moieties, respectively. We show that the anharmonic multi-well character of the orthogonal dyad's intramolecular potential explains findings from both stationary and time-resolved absorption experiments. While for a parallel dyad, standard quantum chemical estimates of J at 0 K are in good agreement with experimental observations, J becomes vanishingly small for the orthogonal dyad, in contrast to its ultrafast experimental transfer times. This discrepancy is not resolved even by accounting for harmonic fluctuations along normal coordinates. We resolve this problem by supplementing quantum chemical approaches with dynamical sampling of fluctuating geometries. In contrast to the moderate Gaussian fluctuations of J for the parallel dyad, fluctuations for the orthogonal dyad are found to follow non-Gaussian statistics leading to significantly higher effective J in good agreement with experimental observations. In effort to apply a unified framework for treating the dynamics of optical coherence and excitonic populations of both dyads, we employ a vibronic approach treating electronic and selected vibrational degrees on an equal footing. This vibronic model is used to model absorption and fluorescence spectra as well as donor-acceptor transport dynamics and covers the more traditional categories of Förster and Redfield transport as limiting cases.

Estimation of Transition-Metal Empirical Parameters for Molecular Mechanical Force Fields.

Force-field parameters of the first row transition metals together with a few additional common elements such as those from the second (Rh, Ru) and third (Hg, Pt) rows of elements in ligated forms were determined based on the density functional theory calculations. Bonding characteristics were determined by averaging metal-ligand force constants in optimal geometries from several chosen complexes of each metal in the most common oxidation numbers and structural arrangements. Parameters of Lennard-Jones potential were determined based on a supermolecular model. Our determined molecular mechanical parameters are compared with presently available parameters published by other groups. We performed two different kinds of testing in order to demonstrate the reliability of these parameters in the case of ligated metallo complexes. First, the nonbonding potential was constructed for an additional set of 19 larger systems containing common complexes with organic molecules. The second test compares the Pt-O and Pt-H radial distribution functions for cisplatin in a box of TIP3P water with lately published studies.