Delocalized electronic excitations and their role in directional charge transfer in the reaction center of Rhodobacter sphaeroides

Abstract

In purple bacteria, the fundamental charge-separation step that drives the conversion of radiation energy into chemical energy proceeds along one branch - the A branch - of a heterodimeric pigment-protein complex, the reaction center. Here, we use first principles time-dependent density functional theory (TDDFT) with an optimally-tuned range-separated hybrid functional to investigate the electronic and excited-state structure of the primary six pigments in the reaction center of \textit{Rhodobacter sphaeroides}. By explicitly including amino-acid residues surrounding these six pigments in our TDDFT calculations, we systematically study the effect of the protein environment on energy and charge-transfer excitations. Our calculations show that a forward charge transfer into the A branch is significantly lower in energy than the first charge transfer into the B branch, in agreement with the unidirectional charge transfer observed experimentally. We further show that inclusion of the protein environment redshifts this excitation significantly, allowing for energy transfer from the coupled $Q_x$ excitations. Through analysis of transition and difference densities, we demonstrate that most of the $Q$-band excitations are strongly delocalized over several pigments and that both their spatial delocalization and charge-transfer character determine how strongly affected they are by thermally-activated molecular vibrations. Our results suggest a mechanism for charge-transfer in this bacterial reaction center and pave the way for further first-principles investigations of the interplay between delocalized excited states, vibronic coupling, and the role of the protein environment of this and other complex light-harvesting systems.

Mapping charge-transfer excitations in Bacteriochlorophyll dimers from first principles

“…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 [64,[87][88][89][90][91][92][93][94][95]. Therefore our results can not directly be used to infer charge-transfer mechanisms in photosynthetic systems.…”

“…Our aim is to assign each grid point of the difference-density grid to its closest pigment molecule. For achieving this, we used the distances between grid points and each molecule's atomic coordinates (including hydrogen atoms), as previously done in [64].…”

“…Two types of BCL dimers constitute our model systems in this study: The first class of dimers (discussed in section 3.1) are extracted from the LHII complex and RC of purple bacteria. We note that the excitation energies that we calculate for these systems will be different from those in vivo, where electrostatic and dielectric effects of the protein environment and coupling with other pigments leads to different excitations and affects locally excited and charge-transfer states differently [34,[64][65][66]. Our goal is to elucidate the factors that determine the energy and character of these excitations, in particular their mixing with the coupled Q y and Q x excitations of the dimers.…”