Understanding Primary Charge Separation in the Heliobacterial Reaction Center

Abstract

The homodimeric reaction center of heliobacteria retains features of the ancestral reaction center and can thus provide insights into the evolution of photosynthesis. Primary charge separation is expected to proceed in a two-step mechanism along either of the two reaction center branches. We reveal the first charge-separation step from first-principles calculations based on time-dependent density functional theory with an optimally tuned rangeseparated hybrid and ab initio Born−Oppenheimer molecular dynamics: the electron is most likely localized on the electron transfer cofactor 3 (EC3, OH-chlorophyll a), and the hole on the adjacent EC2. Including substantial parts of the surrounding protein environment into the calculations shows that a distinct structural mechanism is decisive for the relative energetic positioning of the electronic excitations: specific charged amino acids in the vicinity of EC3 lower the energy of charge-transfer excitations and thus facilitate efficient charge separation. These results are discussed considering recent experimental insights.

Electronic structure and energetics of a heterodimeric BChlg′/Chla′ special pair generated by exposure ofHeliomicrobium modesticaldumto dioxygen

“…It is important to note that this model does not include the A 0 chlorophylls, and recent experimental and theoretical studies suggest that the initial charge separation may occur between the accessory BChl g and A 0 . 47–50 Hence, we need to consider whether or not our findings are consistent with this model. If we assume that conversion of any of the BChl g or BChl g ′ molecules in the electron transfer chain prevents it from acting as an electron donor as suggested by the TD-DFT calculations, the question is then which of the of the BChl g or BChl g ′ molecules must act as an electron donor if long-lived charge separation is to occur.…”

“…Time-dependent density functional theory (TD-DFT) calculations can be applied to study the charge-separated states of the HbRC. 46,47 Such calculations provide vertical excitation energies but do not take the reorganization energy into account. They are also computationally expensive and can only be performed on somewhat restricted models of the RC.…”

Experimental and Theoretical Mutation of Exciton States on the Smallest Type-I Photosynthetic Reaction Center Complex of a Green Sulfur Bacterium Chlorobaclum tepidum

“…Recent structural analyses have also contributed to theoretical studies on the physical processes occurring within type-I RCs. ,,,,− Adolphs et al calculated the excitonic coupling strength between every pair of Chl a molecules on PSI using the Poisson TrESP (P-TrESP) method and obtained the spatial distribution of the site energy shift (SES) values using the charge density coupling (CDC) method. SES values indicate the differences in the electrostatic interactions between the excited and ground states of the Chl a molecules and the surrounding polypeptides.…”