Understanding Primary Charge Separation in the Heliobacterial Reaction Center

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 range-separated 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.