Triplet excitation dynamics of photosynthetic light-harvesting antennae: mechanistic insights into the conjugation regulated carotenoid functionality

Carotenoid (Car) is omnipresent in photosynthetic organisms. The light-harvesting complexes (LHs) of photosynthetic purple bacteria bind Car molecules with a number of conjugated CC double bonds (<i>n</i>_CC) varying from 9 to 13, and the function of Car is accordingly tuned from accessory light harvesting to photoprotection. Car photoprotection is governed by bacteriochlorophyll (BChl)-to-Car triplet excitation transfer (TET), yielding harmless ³Car* <i>via</i> 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 (<i>n</i>_CC = 9-13) for their ³Car* formation dynamics in 0-150 ns with a nanosecond time resolution and found that the TET rate (<i>k</i>_TET) is boosted from (19.45 ns)^-1 to (1.59 ns)^-1 upon systematically increasing <i>n</i>_CC. We show that the essence of TET acceleration is the fine adjustment of the nearest separation between BChl and Car conjugated backbones (<i>R</i>, in Å). Fitting the ln(<i>k</i>_TET)-<i>R</i> plot to Dexter's TET formalism leads to a general rate expression, <i>k</i>_TET = <i>k</i>₀e^-2<i>βR</i>, where <i>k</i>₀ = 2.798 × 10¹² s^-1 and the antennation factor (<i>β</i>) is determined to be 1.28 ± 0.05 Å^-1. Furthermore, we show that the prolongation of Car-conjugation promotes the SF reactivity, whereas it 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 to various light environments.