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

Abstract

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.

Insights into Energy Transfer in Light-Harvesting Complex II Through Machine-Learning Assisted Simulations

“…Trivial diagonalization of the MD-averaged excitonic Hamiltonian is not sufficient, as instant correlations among different sites are completely ignored and the variability of exciton composition is underestimated. Instead, we set our analysis on the “participation ratio” index (PR) averaged over static disorder PR i j = false⟨ ∑ a false| c i a false| 2 false| c j a false| 2 false⟩ normald normali normals where c ia is the excitonic coefficient describing the contribution of site i to exciton a . The PR index is a two-site property which quantifies the probability that two sites participate to the same exciton.…”

“…Linear spectra were calculated with the second-order cumulant expansion of the response function in the secular and Markov approximations . The aggregate spectrum is obtained by summing response contributions from all excitons A ( ω ) ∝ ω ∑ a false| μ 0 a | 2 A a ( ω ) where μ 0 a is the transition dipole transformed to the exciton basis and A a (ω) is the homogeneous lineshape of exciton a A a false( ω false) ∝ R ∫ 0 + ∞ d t e − i false( ω a − ω false) t − g a false( t false) − γ a t Here, γ a is the dephasing term, a complex quantity accounting for exciton relaxation. , Its real part contributes to homogeneous Lorentzian broadening, while its imaginary part shifts the absorption frequency. Its expression in the case of complex Redfield theory is given in the Supporting Information (Section S1).…”

“…We model EET dynamics in LHCII using the combined Redfield-Förster theory. ,, In this framework, the aggregate is split into strongly electronically coupled domains and the Hamiltonian is correspondingly partitioned into blocks. Elements inside the blocks build up the scriptĤ 0 , while between-block elements are moved into a perturbation matrix V ^ , so that scriptĤ = Ĥ 0 + V ^ …”

“…The time dependence of TA is given by the delay time between the pump and the probe pulse, which corresponds to the time interval limited by excitation and probe events left for free evolution. The dynamics of the system during the delay time is described using the Redfield–Förster theory, whereas the excitation and probing events are simulated through a Markovian-secular lineshape theory, , as done for linear absorption. An exact treatment of the response of the system requires consideration of contributions from all elements of the density matrix.…”

“…First-principles strategies are complemented by molecular dynamics (MD) simulations of the complex, which serve to relax the crystal structure toward the solution environment and also allow sampling the ensemble of protein-pigment and pigment–pigment configurations. − Albeit occurring on completely different time scales with respect to the dynamics relevant to EET, protein motions have a direct effect on the energy transfer dynamics, since they cause delocalized electronic states to fluctuate in time. MD-coupled strategies allow capturing these slow fluctuations and accounting for them in the simulation of optical spectra. ,,− The drawback is that (polarizable) QM/MM calculations have to be repeated for a large number of configurations in order to minimize the statistical uncertainty of the results. As a consequence, the cost of these calculations becomes rapidly prohibitive for systems of increasing dimensions.…”