Niedzwiedzki, D.M., Swainsbury, D.J.K. orcid.org/0000-0002-0754-0363, Canniffe, D.P. et al. (2 more authors) (2020) A photosynthetic antenna complex foregoes unity carotenoid-to-bacteriochlorophyll energy transfer efficiency to ensure photoprotection. Proceedings of the National Academy of Sciences, 117 (12). pp. 6502-6508. ISSN 0027-8424
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.
Metadata
Item Type: | Article |
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Authors/Creators: |
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Copyright, Publisher and Additional Information: | © 2020 The Author(s) Published under the PNAS license. This is an author-produced version of a paper subsequently published in Proceedings of the National Academy of Sciences. Uploaded in accordance with the publisher's self-archiving policy. |
Keywords: | photosynthesis; carotenoids; light-harvesting; photoprotection; ultrafast spectroscopy |
Dates: |
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Institution: | The University of Sheffield |
Academic Units: | The University of Sheffield > Faculty of Science (Sheffield) > School of Biosciences (Sheffield) > Department of Molecular Biology and Biotechnology (Sheffield) |
Funding Information: | Funder Grant number BIOTECHNOLOGY AND BIOLOGICAL SCIENCES RESEARCH COUNCIL BB/M000265/1 ENGINEERING AND PHYSICAL SCIENCE RESEARCH COUNCIL EP/S002103/1 |
Depositing User: | Symplectic Sheffield |
Date Deposited: | 17 Apr 2020 16:06 |
Last Modified: | 24 Sep 2020 00:45 |
Status: | Published |
Publisher: | Proceedings of the National Academy of Sciences |
Refereed: | Yes |
Identification Number: | 10.1073/pnas.1920923117 |
Related URLs: | |
Open Archives Initiative ID (OAI ID): | oai:eprints.whiterose.ac.uk:159632 |