Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs

Son, Minjung; Pinnola, Alberta; Gordon, Samuel C.; Bassi, Roberto; Schlau-Cohen, Gabriela S.

doi:10.1038/s41467-020-15074-6

Title: Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs

Journal Article · 10 March 2020 · Nature Communications

DOI: https://doi.org/10.1038/s41467-020-15074-6 · OSTI ID:1619554

^[1]; Pinnola, Alberta ^[2]; Gordon, Samuel C. ^[3];

^[4];

^[1]

Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Chemistry
Univ. of Pavia (Italy). Dept. of Biology and Biotechnology; Univ. of Verona (Italy). Dept. of Biotechnology
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Chemistry; Agenus Inc., Lexington, MA (United States)
Univ. of Verona (Italy). Dept. of Biotechnology; Accademia Nazionale di Lincei, Rome (Italy)

Plants prevent photodamage under high light by dissipating excess energy as heat. Conformational changes of the photosynthetic antenna complexes activate dissipation by leveraging the sensitivity of the photophysics to the protein structure. The mechanisms of dissipation remain debated, largely due to two challenges. First, because of the ultrafast timescales and large energy gaps involved, measurements lacked the temporal or spectral requirements. Second, experiments have been performed in detergent, which can induce nonnative conformations, or in vivo, where contributions from homologous antenna complexes cannot be disentangled. Here, we overcome both challenges by applying ultrabroadband two-dimensional electronic spectroscopy to the principal antenna complex, LHCII, in a near-native membrane. Our data provide evidence that the membrane enhances two dissipative pathways, one of which is a previously uncharacterized chlorophyll-to-carotenoid energy transfer. Our results highlight the sensitivity of the photophysics to local environment, which may control the balance between light harvesting and dissipation in vivo.

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Research Organization:: Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; USDOE

Grant/Contract Number:: SC0018097

OSTI ID:: 1619554

Alternate ID(s):: OSTI ID: 1629981

Journal Information:: Nature Communications, Vol. 11, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Two-Dimensional Electronic Spectroscopy of Light-Harvesting Complex II at Ambient Temperature: A Joint Experimental and Theoretical Study Duan, Hong-Guang; Stevens, Amy L.; Nalbach, Peter The Journal of Physical Chemistry B, Vol. 119, Issue 36 https://doi.org/10.1021/acs.jpcb.5b05592	journal	August 2015
Spectroscopic Properties of Violaxanthin and Lutein Triplet States in LHCII are Independent of Carotenoid Composition Saccon, Francesco; Durchan, Milan; Kaňa, Radek The Journal of Physical Chemistry B, Vol. 123, Issue 44 https://doi.org/10.1021/acs.jpcb.9b06293	journal	October 2019
Single-Molecule Identification of Quenched and Unquenched States of LHCII Schlau-Cohen, Gabriela S.; Yang, Hsiang-Yu; Krüger, Tjaart P. J. The Journal of Physical Chemistry Letters, Vol. 6, Issue 5 https://doi.org/10.1021/acs.jpclett.5b00034	journal	February 2015
LHCII Populations in Different Quenching States Are Present in the Thylakoid Membranes in a Ratio that Depends on the Light Conditions Tian, Lijin; Dinc, Emine; Croce, Roberta The Journal of Physical Chemistry Letters, Vol. 6, Issue 12 https://doi.org/10.1021/acs.jpclett.5b00944	journal	June 2015
Revisiting the Role of Xanthophylls in Nonphotochemical Quenching van Oort, Bart; Roy, Laura M.; Xu, Pengqi The Journal of Physical Chemistry Letters, Vol. 9, Issue 2 https://doi.org/10.1021/acs.jpclett.7b03049	journal	January 2018
Ultrafast Dynamics of Carotenoid Excited States−From Solution to Natural and Artificial Systems Polívka, Tomáš; Sundström, Villy Chemical Reviews, Vol. 104, Issue 4 https://doi.org/10.1021/cr020674n	journal	April 2004
Chlorophyll-Carotenoid Excitation Energy Transfer in High-Light-Exposed Thylakoid Membranes Investigated by Snapshot Transient Absorption Spectroscopy Park, Soomin; Fischer, Alexandra L.; Steen, Collin J. Journal of the American Chemical Society, Vol. 140, Issue 38 https://doi.org/10.1021/jacs.8b04844	journal	September 2018
Identifying the Pathways of Energy Transfer between Carotenoids and Chlorophylls in LHCII and CP29. A Multicolor, Femtosecond Pump−Probe Study Gradinaru, Claudiu C.; van Stokkum, Ivo H. M.; Pascal, Andy A. The Journal of Physical Chemistry B, Vol. 104, Issue 39 https://doi.org/10.1021/jp001752i	journal	October 2000
Correlation of Car S ₁ → Chl with Chl → Car S ₁ Energy Transfer Supports the Excitonic Model in Quenched Light Harvesting Complex II Liao, Pen-Nan; Holleboom, Christoph-Peter; Wilk, Laura The Journal of Physical Chemistry B, Vol. 114, Issue 47 https://doi.org/10.1021/jp1034163	journal	December 2010
Pathways of Energy Flow in LHCII from Two-Dimensional Electronic Spectroscopy Schlau-Cohen, Gabriela S.; Calhoun, Tessa R.; Ginsberg, Naomi S. The Journal of Physical Chemistry B, Vol. 113, Issue 46 https://doi.org/10.1021/jp9066586	journal	November 2009
Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state Barros, Tiago; Royant, Antoine; Standfuss, Jörg The EMBO Journal, Vol. 28, Issue 3 https://doi.org/10.1038/emboj.2008.276	journal	January 2009
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Liu, Zhenfeng; Yan, Hanchi; Wang, Kebin Nature, Vol. 428, Issue 6980 https://doi.org/10.1038/nature02373	journal	March 2004
Identification of a mechanism of photoprotective energy dissipation in higher plants Ruban, Alexander V.; Berera, Rudi; Ilioaia, Cristian Nature, Vol. 450, Issue 7169 https://doi.org/10.1038/nature06262	journal	November 2007
Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection Kondo, Toru; Pinnola, Alberta; Chen, Wei Jia Nature Chemistry, Vol. 9, Issue 8 https://doi.org/10.1038/nchem.2818	journal	July 2017
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Plant carotenoids: recent advances and future perspectives Sun, Tianhu; Rao, Sombir; Zhou, Xuesong Molecular Horticulture, Vol. 2, Issue 1 https://doi.org/10.1186/s43897-022-00023-2	journal	January 2022

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