Stéphanie Valleau

Atomistic Study of the Long-Lived Quantum Coherences in the Fenna-Matthews-Olson Complex

A remarkable amount of theoretical research has been carried out to elucidate the physical origins of the recently observed long-lived quantum coherence in the electronic energy transfer process in biological photosynthetic systems. Although successful in many respects, several widely used descriptions only include an effective treatment of the protein-chromophore interactions. In this work, by combining an all-atom molecular dynamics simulation, time-dependent density functional theory, and open quantum system approaches, we successfully simulate the dynamics of the electronic energy transfer of the Fenna-Matthews-Olson pigment-protein complex. The resulting characteristic beating of populations and quantum coherences is in good agreement with the experimental results and the hierarchy equation of motion approach. The experimental absorption, linear, and circular dichroism spectra and dephasing rates are recovered at two different temperatures. In addition, we provide an extension of our method to include zero-point fluctuations of the vibrational environment. This work thus presents, to our knowledge, one of the first steps to explain the role of excitonic quantum coherence in photosynthetic light-harvesting complexes based on their atomistic and molecular description.

Photonics meets excitonics: natural and artificial molecular aggregates

Abstract Organic molecules store the energy of absorbed light in the form of charge-neutral molecular excitations – Frenkel excitons. Usually, in amorphous organic materials, excitons are viewed as quasiparticles, localized on single molecules, which diffuse randomly through the structure. However, the picture of incoherent hopping is not applicable to some classes of molecular aggregates – assemblies of molecules that have strong near-field interaction between electronic excitations in the individual subunits. Molecular aggregates can be found in nature, in photosynthetic complexes of plants and bacteria, and they can also be produced artificially in various forms including quasi-one dimensional chains, two-dimensional films, tubes, etc. In these structures light is absorbed collectively by many molecules and the following dynamics of molecular excitation possesses coherent properties. This energy transfer mechanism, mediated by the coherent exciton dynamics, resembles the propagation of electromagnetic waves through a structured medium on the nanometer scale. The absorbed energy can be transferred resonantly over distances of hundreds of nanometers before exciton relaxation occurs. Furthermore, the spatial and energetic landscape of molecular aggregates can enable the funneling of the exciton energy to a small number of molecules either within or outside the aggregate. In this review we establish a bridge between the fields of photonics and excitonics by describing the present understanding of exciton dynamics in molecular aggregates.

Atomistic Study of Energy Funneling in the Light-Harvesting Complex of Green Sulfur Bacteria

Phototrophic organisms such as plants, photosynthetic bacteria, and algae use microscopic complexes of pigment molecules to absorb sunlight. Within the light-harvesting complexes, which frequently have several functional and structural subunits, the energy is transferred in the form of molecular excitations with very high efficiency. Green sulfur bacteria are considered to be among the most efficient light-harvesting organisms. Despite multiple experimental and theoretical studies of these bacteria, the physical origin of the efficient and robust energy transfer in their light-harvesting complexes is not well understood. To study excitation dynamics at the systems level, we introduce an atomistic model that mimics a complete light-harvesting apparatus of green sulfur bacteria. The model contains approximately 4000 pigment molecules and comprises a double wall roll for the chlorosome, a baseplate, and six Fenna-Matthews-Olson trimer complexes. We show that the fast relaxation within functional subunits combined with the transfer between collective excited states of pigments can result in robust energy funneling to the initial excitation conditions and temperature changes. Moreover, the same mechanism describes the coexistence of multiple time scales of excitation dynamics frequently observed in ultrafast optical experiments. While our findings support the hypothesis of supertransfer, the model reveals energy transport through multiple channels on different length scales.

Exciton transport in thin-film cyanine dye J-aggregates

We present a theoretical model for the study of exciton dynamics in J-aggregated monolayers of fluorescent dyes. The excitonic evolution is described by a Monte-Carlo wave function approach which allows for a unified description of the quantum (ballistic) and classical (diffusive) propagation of an exciton on a lattice in different parameter regimes. The transition between the ballistic and diffusive regime is controlled by static and dynamic disorder. As an example, the model is applied to three cyanine dye J-aggregates: TC, TDBC, and U3. Each of the molecule-specific structure and excitation parameters are estimated using time-dependent density functional theory. The exciton diffusion coefficients are calculated and analyzed for different degrees of film disorder and are correlated to the physical properties and the structural arrangement of molecules in the aggregates. Further, exciton transport is anisotropic and dependent on the initial exciton energy. The upper-bound estimation of the exciton diffusion length in the TDBC thin-film J-aggregate is of the order of hundreds of nanometers, which is in good qualitative agreement with the diffusion length estimated from experiments.

Influence of Force Fields and Quantum Chemistry Approach on Spectral Densities of BChl a in Solution and in FMO Proteins

Studies on light-harvesting (LH) systems have attracted much attention after the finding of long-lived quantum coherences in the exciton dynamics of the Fenna-Matthews-Olson (FMO) complex. In this complex, excitation energy transfer occurs between the bacteriochlorophyll a (BChl a) pigments. Two quantum mechanics/molecular mechanics (QM/MM) studies, each with a different force-field and quantum chemistry approach, reported different excitation energy distributions for the FMO complex. To understand the reasons for these differences in the predicted excitation energies, we have carried out a comparative study between the simulations using the CHARMM and AMBER force field and the Zerner intermediate neglect of differential orbital (ZINDO)/S and time-dependent density functional theory (TDDFT) quantum chemistry methods. The calculations using the CHARMM force field together with ZINDO/S or TDDFT always show a wider spread in the energy distribution compared to those using the AMBER force field. High- or low-energy tails in these energy distributions result in larger values for the spectral density at low frequencies. A detailed study on individual BChl a molecules in solution shows that without the environment, the density of states is the same for both force field sets. Including the environmental point charges, however, the excitation energy distribution gets broader and, depending on the applied methods, also asymmetric. The excitation energy distribution predicted using TDDFT together with the AMBER force field shows a symmetric, Gaussian-like distribution.

Machine learning exciton dynamics

Machine learning ground state QM/MM for accelerated computation of exciton dynamics.

First Principles Semiclassical Calculations of Vibrational Eigenfunctions

Vibrational eigenfunctions are calculated on-the-fly using semiclassical methods in conjunction with ab initio density functional theory classical trajectories. Various semiclassical approximations based on the time-dependent representation of the eigenfunctions are tested on an analytical potential describing the chemisorption of CO on Cu(100). Then, first principles semiclassical vibrational eigenfunctions are calculated for the CO(2) molecule and its accuracy evaluated. The multiple coherent states initial value representations semiclassical method recently developed by us has shown with only six ab initio trajectories to evaluate eigenvalues and eigenfunctions at the accuracy level of thousands trajectory semiclassical initial value representation simulations.

Electromagnetic study of the chlorosome antenna complex of Chlorobium tepidum.

Green sulfur bacteria are an iconic example of natures adaptation: thriving in environments of extremely low photon density, the bacterium ranks itself among the most efficient natural light-harvesting organisms. The photosynthetic antenna complex of this bacterium is a self-assembled nanostructure, ≈60 × 150 nm, made of bacteriochlorophyll molecules. We study the system from a computational nanoscience perspective by using electrodynamic modeling with the goal of understanding its role as a nanoantenna. Three different nanostructures, built from two molecular packing moieties, are considered: a structure built of concentric cylinders of aggregated bacteriochlorophyll d monomers, a single cylinder of bacteriochlorophyll c monomers, and a model for the entire chlorosome. The theoretical model captures both coherent and incoherent components of exciton transfer. The model is employed to extract optical spectra, concentration and depolarization of electromagnetic fields within the chlorosome, and fluxes of energy transfer for the structures. The second model nanostructure shows the largest field enhancement. Further, field enhancement is found to be more sensitive to dynamic noise rather than structural disorder. Field depolarization, however, is similar for all structures. This indicates that the directionality of transfer is robust to structural variations, while on the other hand, the intensity of transfer can be tuned by structural variations.

Absence of Selection for Quantum Coherence in the Fenna–Matthews–Olson Complex: A Combined Evolutionary and Excitonic Study

We present a study on the evolution of the Fenna–Matthews–Olson bacterial photosynthetic pigment–protein complex. This protein complex functions as an antenna. It transports absorbed photons—excitons—to a reaction center where photosynthetic reactions initiate. The efficiency of exciton transport is therefore fundamental for the photosynthetic bacterium’s survival. We have reconstructed an ancestor of the complex to establish whether coherence in the exciton transport was selected for or optimized over time. We have also investigated the role of optimizing free energy variation upon folding in evolution. We studied whether mutations which connect the ancestor to current day species were stabilizing or destabilizing from a thermodynamic viewpoint. From this study, we established that most of these mutations were thermodynamically neutral. Furthermore, we did not see a large change in exciton transport efficiency or coherence, and thus our results predict that exciton coherence was not specifically selected for.

Parametric Hierarchical Matrix Approach for the Wideband Optical Response of Large-Scale Molecular Aggregates

Fast and efficient calculations of optical responses using electromagnetic models require computational acceleration and compression techniques. A hierarchical matrix approach is adopted for this purpose. In order to model large-scale molecular structures, these methods should be applied over wide frequency spectra. Here, we introduce a novel parametric hierarchical matrix method that allows one for a rapid construction of a wideband system representation and enables an efficient wideband solution. We apply the developed method to the modeling of the optical response of bacteriochlorophyll tubular aggregates as found in green photosynthetic bacteria. We show that the parametric method can provide one with the frequency and time-domain solutions for structures of the size of 100 000 molecules, which is comparable to the size of the whole antenna complex in a bacterium. The absorption spectrum is calculated and the significance of electrodynamic retardation effects for relatively large structures, i.e., wit...