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

Niedzwiedzki, Dariusz M., Swainsbury, David J.K., Canniffe, Daniel P., Neil Hunter, C. 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 the United States of America, 117 (12). pp. 6502-6508. ISSN 0027-8424

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Abstract

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
Additional Information: Funding Information: Spectroscopic work was performed at the Ultrafast Laser Facility of the Center for Solar Energy and Energy Storage at Washington University in Saint Louis. D.M.N. acknowledges the Center for Solar Energy and Energy Storage at McKelvey School of Engineering at Washington University in Saint Louis for financial support. D.J.K.S., D.P.C., C.N.H., and A.H. were supported by the Biotechnology and Biological Sciences Research Council award number BB/M000265/1. C.N.H. further acknowledges award number EP/S002103/1 from the Engineering and Physical Sciences Research Council. A.H. also acknowledges support from a Royal Society University Research Fellowship (award number URF\R1\191548). Funding Information: ACKNOWLEDGMENTS. Spectroscopic work was performed at the Ultrafast Laser Facility of the Center for Solar Energy and Energy Storage at Washington University in Saint Louis. D.M.N. acknowledges the Center for Solar Energy and Energy Storage at McKelvey School of Engineering at Washington University in Saint Louis for financial support. D.J.K.S., D.P.C., C.N.H., and A.H. were supported by the Biotechnology and Biological Sciences Research Council award number BB/M000265/1. C.N.H. further acknowledges award number EP/S002103/1 from the Engineering and Physical Sciences Research Council. A.H. also acknowledges support from a Royal Society University Research Fellowship (award number URF\R1\191548). Publisher Copyright: © 2020 National Academy of Sciences. All rights reserved.
Uncontrolled Keywords: carotenoids,light-harvesting,photoprotection,photosynthesis,ultrafast spectroscopy,general ,/dk/atira/pure/subjectarea/asjc/1000
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 17 Aug 2022 12:31
Last Modified: 24 Sep 2022 07:04
URI: https://ueaeprints.uea.ac.uk/id/eprint/87358
DOI: 10.1073/pnas.1920923117

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