A photosynthetic antenna complex foregoes unity carotenoid-to-bacteriochlorophyll energy transfer efficiency to ensure photoprotection

Niedzwiedzki, Dariusz M, Swainsbury, David JK, Canniffe, Daniel P ORCID: 0000-0002-5022-0437, Hunter, C Neil and Hitchcock, Andrew
(2020) A photosynthetic antenna complex foregoes unity carotenoid-to-bacteriochlorophyll energy transfer efficiency to ensure photoprotection. Proceedings of the National Academy of Sciences of USA, 117 (12). pp. 6502-6508.

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Carotenoids play a number of important roles in photosynthesis, primarily providing light-harvesting and photoprotective energy dissipation functions within pigment–protein complexes. The carbon–carbon double bond (C=C) conjugation length of carotenoids (N), generally between 9 and 15, determines the carotenoid-to-(bacterio)chlorophyll [(B)Chl] energy transfer efficiency. Here we purified and spectroscopically characterized light-harvesting complex 2 (LH2) from Rhodobacter sphaeroides containing the N = 7 carotenoid zeta (ζ)-carotene, not previously incorporated within a natural antenna complex. Transient absorption and time-resolved fluorescence show that, relative to the lifetime of the S1 state of ζ-carotene in solvent, the lifetime decreases ∼250-fold when ζ-carotene is incorporated within LH2, due to transfer of excitation energy to the B800 and B850 BChls a. These measurements show that energy transfer proceeds with an efficiency of ∼100%, primarily via the S1 → Qx route because the S1 → S0 fluorescence emission of ζ-carotene overlaps almost perfectly with the Qx absorption band of the BChls. However, transient absorption measurements performed on microsecond timescales reveal that, unlike the native N ≥ 9 carotenoids normally utilized in light-harvesting complexes, ζ-carotene does not quench excited triplet states of BChl a, likely due to elevation of the ζ-carotene triplet energy state above that of BChl a. These findings provide insights into the coevolution of photosynthetic pigments and pigment–protein complexes. We propose that the N ≥ 9 carotenoids found in light-harvesting antenna complexes represent a vital compromise that retains an acceptable level of energy transfer from carotenoids to (B)Chls while allowing acquisition of a new, essential function, namely, photoprotective quenching of harmful (B)Chl triplets.

Item Type: Article
Uncontrolled Keywords: photosynthesis, carotenoids, light-harvesting, photoprotection, ultrafast spectroscopy
Depositing User: Symplectic Admin
Date Deposited: 01 May 2020 10:31
Last Modified: 18 Jan 2023 23:54
DOI: 10.1073/pnas.1920923117
Related URLs:
URI: https://livrepository.liverpool.ac.uk/id/eprint/3083621