Triplet Excitation Dynamics of Photosynthetic Light-Harvesting Antennae: Mechanistic Insights into the Conjugation Regulated Carotenoid Functionality

Abstract

Carotenoid (Car) is omnipresent in photosynthetic organisms. The light-harvesting complexes (LHs) of photosynthetic purple bacteria bind Car molecules with the number of conjugated C=C double bonds (n_c=c) varying from 9 to 13, and the function of Car is accordingly tunned from accessary light harvesting to photoprotection. Car photoprotection is governed by bacteriochlorophyll (BChl)-to-Car triplet excitation transfer (TET), yielding harmless ³Car* via quenching the unwanted ³BChl*. Meanwhile, Car on direct photoexcitation may experience ultrafast singlet fission (SF), in effect deactivating ¹Car* while yielding ³Car* albeit the elusive physiological significance. We have attempted to explore the molecular mechanism underlying the conjugation dependence of Car functionality. To this end, we examined 10 different kinds of LHs binding Cars of different conjugation lengths (n_c=c = 9–13) for their ³Car* formation dynamics in 0–150 ns with a nanosecond time resolution and found that the TET rate (k_TET) is boosted from (19.45 ns)^-1 to (1.59 ns)^-1 upon systematically increasing n_c=c. We show that the essence of TET acceleration is the fine adjustment of the nearest separation between BChl and Car conjugated backbones (R). Fitting the ln(k_TET)-R plot to Dexter’s TET formulism leads to a general rate expression, k_TET = 2798 e^-2bR (ns^-1), wherein the antennation factor (b) is determined to be 1.28 ± 0.05 Å^-1. Furthermore, we show that prolongation of Car-conjugation promotes the SF reactivity, whereas concurrently reduces the efficiency of Car-to-BChl singlet energy transfer. The results are discussed in terms of Car-conjugation regulated photoprotection for photosynthetic bacteria to acclimate various light environment.