Molecular basis for alternative charge separation pathways in type-II photosynthetic reaction centers

Abstract In photosynthetic reaction centers from purple bacteria, bacteriochlorophyll a (the special pair PAPB and accessory bacteriochlorophyll BA) and bacteriopheophytin a (HA) form the active electron-transfer branch and uniquely contain a polar methyl-keto (3-acetyl) group. However, despite its importance in defining local polarity, even the currently available highest-resolution structures (∼2 Å) cannot unambiguously distinguish the methyl carbon from the keto oxygen, limiting insight into its functional role. Here, we investigate how the methyl-keto orientations of the PB and HA cofactors influence the energetics of charge-separated intermediates, using a quantum mechanical/molecular mechanical approach. We identify two kinetically isolated, metastable methyl-keto conformations of PB, Tyr-OH…BA and Tyr-OH…PB, each associated with a distinct charge-separation pathway: the canonical [PAPB]* → [PAPB]•+BA•− and alternative BA* → BA•+HA•− pathways, respectively. For HA, methyl-keto reorientation stabilizes HA•− when forward transfer to the primary quinone (QA) is inhibited. These results show that distinct methyl-keto conformations selectively tune charge-separation routes while also contributing to the oxidative robustness of bacteriochlorin macrocycles.