Investigating Primary Charge Separation in the Reaction Center of Heliobacterium modesticaldum

Abstract

We compute the primary charge separation step in the homodimeric reaction center (RC) of Heliobacterium modesticaldum from first principles. Using time-dependent density functional theory with the optimally tuned range-separated hybrid functional ωPBE, we calculate the excitations of a system comprising the special pair, the adjacent accessory bacteriochlorophylls, and the most relevant parts of the surrounding protein environment. The structure of the excitation spectrum can be rationalized from coupling of the individual bacteriochlorophyll pigments similar to molecular J- and H-aggregates. We find excited states corresponding to forward-charge transfer along the individual branches of the RC of H. modesticaldum. In the spectrum, these are located at an energy between the coupled Q y and Q x transitions. With ab initio Born–Oppenheimer molecular dynamics simulations, we reveal the influence of thermal vibrations on the excited states. The results show that the energy gap between the coupled Q y and the forward-charge transfer excitations is ∼0.4 eV, which we consider to conflict with the concept of a direct transfer mechanism. Our calculations, however, reveal a certain spectral overlap of the forward-charge transfer and the coupled Q x excitations. The reliability and robustness of the results are demonstrated by several numerical tests.

Understanding Primary Charge Separation in the Heliobacterial Reaction Center

“…Very strikingly, most of the EC2 + EC3 – counts are around or slightly below the center of the Q y band whereas the SPP + EC3 – and SPP + EC2 – excitations are found mostly above this band. Especially, there is a gap of ≳0.3 eV between the center of the Q y band and the SPP + EC2 – excitations, in agreement with our previous work . This outcome clearly suggests that the SPP + EC2 – states presumably do not participate in primary charge separation, while EC2 + EC3 – is a likely candidate for the first charge-separated state.…”

“…Kimura and co-workers − have investigated the excitonic coupling of the chromophores in the RC complex via model Hamiltonian approaches. In our previous work we have calculated the CT states of a reduced system of SPP and EC2. In this work, we take a further step forward and consider the full charge separation branches of the heliobacterial RC in a study based on time-dependent density functional theory (TDDFT) and Born–Oppenheimer molecular dynamics (BOMD).…”

“…We have checked that this is sufficient to reproduce the relevant excited-state properties (in terms of primary charge separation) of the whole two branches. In all calculations we additionally include a few amino acids (histidine, glutamine, serine, and phenylalanine) and waters that coordinate the BChls and Chls and are known to have a relevant influence on the excited states . These molecules are displayed along with the chromophores in Figure a (upper part).…”

“…The total spectrum exhibits two peaks: the first one at 1.7 to 1.8 eV arises predominantly from the Q y excitations of the BChl g pigments; the second one at 2.1 to 2.2 eV comes from the Q y excitations of EC3 and the Q x excitations of the BChl g pigments. Compared to the excitation spectrum of the crystal structure, the ensemble-averaged spectrum is blue-shifted by ∼0.2 eV . Although the main focus of this work is to describe the CT properties of the heliobacterial RC appropriately rather than to reproduce all details of the experimental absorption spectrum, ,, one might want to compare the calculated results to the experimental data.…”

Mapping Charge-Transfer Excitations in Bacteriochlorophyll Dimers from First Principles

“…In vivo, i.e., within the evolutionary-optimized protein networks of the photosynthetic apparatus, the protein environment determines the distance, orientation, and structural details of these aggregates. Furthermore, the protein environment indirectly affects the excited state structure and dynamics of BCL aggregates through dielectric screening and electrostatic effects [75,81,82,[82][83][84][85][86][87][88][89]. Therefore our results can not directly be used to infer charge-transfer mechanisms in photosynthetic systems Nonetheless, they provide an intuitive understanding and design rules for tailoring charge-transfer excitations in BCLs and similar photoactive molecules.…”