Singlet fission mediates carotenoid-to-bacteriochlorophyll energy transfer in purple photosynthetic bacteria

Abstract

Photosynthesis, the foundation of most life, begins when sunlight is captured by (bacterio)chlorophyll ((B)Chl) and carotenoid (Crt) pigments. These molecules are arranged so that captured energy migrates rapidly to reaction centres, where it is stored as a charge separation. The complementary absorption of Crt and (B)Chl pigments, and rapid energy transfer between them, underpins solar harvesting. Here we report a Crt-to-BChl energy transfer mechanism mediated by singlet fission, in which a high-energy singlet exciton (with spin quantum number S = 0) is converted into two low-energy triplet (S = 1) excitons. In purple photosynthetic bacteria, the Crt S2 singlet exciton splits into Crt and BChl triplet excitons on adjacent sites. Once formed, the triplets transfer cooperatively to BChl and onwards to reaction centres. Energy is transferred from a singlet Crt state, via the spin-protected long-lived triplet pair, to a singlet BChl state. Thus, this singlet fission-mediated mechanism augments solar energy harvesting for photosynthesis. The biological role of singlet fission—where two excitons are generated by one photon—is poorly understood. Now it has been shown that heterofission occurs in bacterial light-harvesting complexes, creating a triplet-pair reservoir that enhances carotenoid-to-bacteriochlorophyll energy transfer efficiency and temporarily staggers energy delivery to the reaction centre.