Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs
Abstract
Abstract 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 non-native 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.
- Publication Date:
- Research Org.:
- Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
- OSTI Identifier:
- 1619554
- Alternate Identifier(s):
- OSTI ID: 1629981
- Grant/Contract Number:
- SC0018097
- Resource Type:
- Published Article
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Name: Nature Communications Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Son, Minjung, Pinnola, Alberta, Gordon, Samuel C., Bassi, Roberto, and Schlau-Cohen, Gabriela S. Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs. United Kingdom: N. p., 2020.
Web. doi:10.1038/s41467-020-15074-6.
Son, Minjung, Pinnola, Alberta, Gordon, Samuel C., Bassi, Roberto, & Schlau-Cohen, Gabriela S. Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs. United Kingdom. https://doi.org/10.1038/s41467-020-15074-6
Son, Minjung, Pinnola, Alberta, Gordon, Samuel C., Bassi, Roberto, and Schlau-Cohen, Gabriela S. Tue .
"Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs". United Kingdom. https://doi.org/10.1038/s41467-020-15074-6.
@article{osti_1619554,
title = {Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs},
author = {Son, Minjung and Pinnola, Alberta and Gordon, Samuel C. and Bassi, Roberto and Schlau-Cohen, Gabriela S.},
abstractNote = {Abstract 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 non-native 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.},
doi = {10.1038/s41467-020-15074-6},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United Kingdom},
year = {Tue Mar 10 00:00:00 EDT 2020},
month = {Tue Mar 10 00:00:00 EDT 2020}
}
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Works referenced in this record:
Quantum coherence and its interplay with protein environments in photosynthetic electronic energy transfer
journal, January 2010
- Ishizaki, Akihito; Calhoun, Tessa R.; Schlau-Cohen, Gabriela S.
- Physical Chemistry Chemical Physics, Vol. 12, Issue 27
Pigment Interactions in Light-harvesting Complex II in Different Molecular Environments
journal, December 2014
- Akhtar, Parveen; Dorogi, Márta; Pawlak, Krzysztof
- Journal of Biological Chemistry, Vol. 290, Issue 8
Chlorophyll-Carotenoid Excitation Energy Transfer in High-Light-Exposed Thylakoid Membranes Investigated by Snapshot Transient Absorption Spectroscopy
journal, September 2018
- Park, Soomin; Fischer, Alexandra L.; Steen, Collin J.
- Journal of the American Chemical Society, Vol. 140, Issue 38
Snapshot Transient Absorption Spectroscopy of Carotenoid Radical Cations in High-Light-Acclimating Thylakoid Membranes
journal, November 2017
- Park, Soomin; Fischer, Alexandra L.; Li, Zhirong
- The Journal of Physical Chemistry Letters, Vol. 8, Issue 22
Control of the light harvesting function of chloroplast membranes: The LHCII-aggregation model for non-photochemical quenching
journal, July 2005
- Horton, Peter; Wentworth, Mark; Ruban, Alexander
- FEBS Letters, Vol. 579, Issue 20
Identifying the Pathways of Energy Transfer between Carotenoids and Chlorophylls in LHCII and CP29. A Multicolor, Femtosecond Pump−Probe Study
journal, October 2000
- Gradinaru, Claudiu C.; van Stokkum, Ivo H. M.; Pascal, Andy A.
- The Journal of Physical Chemistry B, Vol. 104, Issue 39
Capturing the Quenching Mechanism of Light-Harvesting Complexes of Plants by Zooming in on the Ensemble
journal, November 2019
- Mascoli, Vincenzo; Liguori, Nicoletta; Xu, Pengqi
- Chem, Vol. 5, Issue 11
Time-resolved fluorescence measurements on leaves: principles and recent developments
journal, November 2018
- Chukhutsina, Volha U.; Holzwarth, Alfred R.; Croce, Roberta
- Photosynthesis Research, Vol. 140, Issue 3
Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis
journal, September 1994
- Frank, Harry A.; Cua, Agnes; Chynwat, Veeradej
- Photosynthesis Research, Vol. 41, Issue 3
Time-Resolved Fluorescence Analysis of the Photosystem II Antenna Proteins in Detergent Micelles and Liposomes †
journal, October 2001
- Moya, Ismael; Silvestri, Mariuccia; Vallon, Olivier
- Biochemistry, Vol. 40, Issue 42
Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants
journal, October 2017
- Balevičius, Vytautas; Fox, Kieran F.; Bricker, William P.
- Scientific Reports, Vol. 7, Issue 1
Understanding the Changes in the Circular Dichroism of Light Harvesting Complex II upon Varying Its Pigment Composition and Organization †
journal, April 2007
- Georgakopoulou, Sofia; van der Zwan, Gert; Bassi, Roberto
- Biochemistry, Vol. 46, Issue 16
Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting
journal, April 2003
- Ma, Y. -Z.; Holt, N. E.; Li, X. -P.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 8
Disentangling protein and lipid interactions that control a molecular switch in photosynthetic light harvesting
journal, January 2017
- Crisafi, Emanuela; Pandit, Anjali
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1859, Issue 1
Single-Molecule Identification of Quenched and Unquenched States of LHCII
journal, February 2015
- Schlau-Cohen, Gabriela S.; Yang, Hsiang-Yu; Krüger, Tjaart P. J.
- The Journal of Physical Chemistry Letters, Vol. 6, Issue 5
An ‘all pigment’ model of excitation quenching in LHCII
journal, January 2015
- Chmeliov, Jevgenij; Bricker, William P.; Lo, Cynthia
- Physical Chemistry Chemical Physics, Vol. 17, Issue 24
Pathways of energy transfer in LHCII revealed by room-temperature 2D electronic spectroscopy
journal, January 2014
- Wells, Kym L.; Lambrev, Petar H.; Zhang, Zhengyang
- Phys. Chem. Chem. Phys., Vol. 16, Issue 23
Equilibrium between Quenched and Nonquenched Conformations of the Major Plant Light-Harvesting Complex Studied with High-Pressure Time-Resolved Fluorescence
journal, July 2007
- van Oort, Bart; van Hoek, Arie; Ruban, Alexander V.
- The Journal of Physical Chemistry B, Vol. 111, Issue 26
Linear dichroism and circular dichroism in photosynthesis research
journal, May 2009
- Garab, Győző; van Amerongen, Herbert
- Photosynthesis Research, Vol. 101, Issue 2-3
The Electronic Structure of Lutein 2 Is Optimized for Light Harvesting in Plants
journal, March 2019
- Son, Minjung; Pinnola, Alberta; Bassi, Roberto
- Chem, Vol. 5, Issue 3
Revisiting the Role of Xanthophylls in Nonphotochemical Quenching
journal, January 2018
- van Oort, Bart; Roy, Laura M.; Xu, Pengqi
- The Journal of Physical Chemistry Letters, Vol. 9, Issue 2
Fluorescence Spectral Dynamics of Single LHCII Trimers
journal, June 2010
- Krüger, Tjaart P. J.; Novoderezhkin, Vladimir I.; Ilioaia, Cristian
- Biophysical Journal, Vol. 98, Issue 12
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria
book, January 2014
- Demmig-Adams, Barbara; Garab, Gyozo; Adams III, William
- Advances in Photosynthesis and Respiration
Far-red fluorescence: A direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching
journal, October 2008
- Miloslavina, Yuliya; Wehner, Antje; Lambrev, Petar H.
- FEBS Letters, Vol. 582, Issue 25-26
Assembly of the Major Light-Harvesting Complex II in Lipid Nanodiscs
journal, November 2011
- Pandit, Anjali; Shirzad-Wasei, Nazhat; Wlodarczyk, Lucyna M.
- Biophysical Journal, Vol. 101, Issue 10
Carotenoid-Bacteriochlorophyll Energy Transfer in LH2 Complexes Studied with 10-fs Time Resolution
journal, April 2006
- Polli, Dario; Cerullo, Giulio; Lanzani, Guglielmo
- Biophysical Journal, Vol. 90, Issue 7
Ultrafast Dynamics of Carotenoid Excited States−From Solution to Natural and Artificial Systems
journal, April 2004
- Polívka, Tomáš; Sundström, Villy
- Chemical Reviews, Vol. 104, Issue 4
Ultrafast excited state relaxation in long-chain polyenes
journal, July 2010
- Antognazza, Maria Rosa; Lüer, Larry; Polli, Dario
- Chemical Physics, Vol. 373, Issue 1-2
Zwischenmolekulare Energiewanderung und Fluoreszenz
journal, January 1948
- Förster, Th.
- Annalen der Physik, Vol. 437, Issue 1-2, p. 55-75
Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting
journal, January 2005
- Holt, N. E.
- Science, Vol. 307, Issue 5708
Different carotenoid conformations have distinct functions in light-harvesting regulation in plants
journal, December 2017
- Liguori, Nicoletta; Xu, Pengqi; van Stokkum, Ivo H. M.
- Nature Communications, Vol. 8, Issue 1
Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection
journal, July 2017
- Kondo, Toru; Pinnola, Alberta; Chen, Wei Jia
- Nature Chemistry, Vol. 9, Issue 8
Nanodiscs in Membrane Biochemistry and Biophysics
journal, February 2017
- Denisov, Ilia G.; Sligar, Stephen G.
- Chemical Reviews, Vol. 117, Issue 6
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution
journal, March 2004
- Liu, Zhenfeng; Yan, Hanchi; Wang, Kebin
- Nature, Vol. 428, Issue 6980
Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein
journal, May 2008
- Ahn, T. K.; Avenson, T. J.; Ballottari, M.
- Science, Vol. 320, Issue 5877
Chlorophyll Binding to Monomeric Light-harvesting Complex: A MUTATION ANALYSIS OF CHROMOPHORE-BINDING RESIDUES
journal, November 1999
- Remelli, Rosaria; Varotto, Claudio; Sandonà, Dorianna
- Journal of Biological Chemistry, Vol. 274, Issue 47
Direct interaction of the major light-harvesting complex II and PsbS in nonphotochemical quenching
journal, March 2013
- Wilk, L.; Grunwald, M.; Liao, P. -N.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 14
Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes
journal, August 2011
- Kruger, T. P. J.; Wientjes, E.; Croce, R.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 33
On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls
journal, July 2009
- Bode, S.; Quentmeier, C. C.; Liao, P. -N.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 30
Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins
journal, February 2015
- Staleva, Hristina; Komenda, Josef; Shukla, Mahendra K.
- Nature Chemical Biology, Vol. 11, Issue 4
Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state
journal, January 2009
- Barros, Tiago; Royant, Antoine; Standfuss, Jörg
- The EMBO Journal, Vol. 28, Issue 3
Ultrabroadband 2D electronic spectroscopy with high-speed, shot-to-shot detection
journal, January 2017
- Son, Minjung; Mosquera-Vázquez, Sandra; Schlau-Cohen, Gabriela S.
- Optics Express, Vol. 25, Issue 16
Spectroscopic Properties of Violaxanthin and Lutein Triplet States in LHCII are Independent of Carotenoid Composition
journal, October 2019
- Saccon, Francesco; Durchan, Milan; Kaňa, Radek
- The Journal of Physical Chemistry B, Vol. 123, Issue 44
Effect of xanthophyll composition on the chlorophyll excited state lifetime in plant leaves and isolated LHCII
journal, July 2010
- Johnson, Matthew P.; Zia, Ahmad; Horton, Peter
- Chemical Physics, Vol. 373, Issue 1-2
Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis
journal, June 2013
- Niyogi, Krishna K.; Truong, Thuy B.
- Current Opinion in Plant Biology, Vol. 16, Issue 3
Identification of a mechanism of photoprotective energy dissipation in higher plants
journal, November 2007
- Ruban, Alexander V.; Berera, Rudi; Ilioaia, Cristian
- Nature, Vol. 450, Issue 7169
Impact of the lipid bilayer on energy transfer kinetics in the photosynthetic protein LH2
journal, January 2018
- Ogren, John I.; Tong, Ashley L.; Gordon, Samuel C.
- Chemical Science, Vol. 9, Issue 12
Two-Dimensional Electronic Spectroscopy of Light-Harvesting Complex II at Ambient Temperature: A Joint Experimental and Theoretical Study
journal, August 2015
- Duan, Hong-Guang; Stevens, Amy L.; Nalbach, Peter
- The Journal of Physical Chemistry B, Vol. 119, Issue 36
Theoretical study of vibrational relaxation and internal conversion dynamics of chlorophyll-a in ethyl acetate solvent in femtosecond laser fields
journal, December 2006
- Dong, Li-Qing; Niu, Kai; Cong, Shu-Lin
- Chemical Physics Letters, Vol. 432, Issue 1-3
Molecular basis of photoprotection and control of photosynthetic light-harvesting
journal, July 2005
- Pascal, Andrew A.; Liu, Zhenfeng; Broess, Koen
- Nature, Vol. 436, Issue 7047
The nature of self-regulation in photosynthetic light-harvesting antenna
journal, April 2016
- Chmeliov, Jevgenij; Gelzinis, Andrius; Songaila, Egidijus
- Nature Plants, Vol. 2, Issue 5
Correlation of Car S 1 → Chl with Chl → Car S 1 Energy Transfer Supports the Excitonic Model in Quenched Light Harvesting Complex II
journal, December 2010
- Liao, Pen-Nan; Holleboom, Christoph-Peter; Wilk, Laura
- The Journal of Physical Chemistry B, Vol. 114, Issue 47
From isolated light-harvesting complexes to the thylakoid membrane: a single-molecule perspective
journal, January 2018
- Gruber, J. Michael; Malý, Pavel; Krüger, Tjaart P. J.
- Nanophotonics, Vol. 7, Issue 1
Carotenoid Radical Cations as a Probe for the Molecular Mechanism of Nonphotochemical Quenching in Oxygenic Photosynthesis
journal, April 2007
- Amarie, Sergiu; Standfuss, Jörg; Barros, Tiago
- The Journal of Physical Chemistry B, Vol. 111, Issue 13
The Major Antenna Complex of Photosystem II Has a Xanthophyll Binding Site Not Involved in Light Harvesting
journal, July 2001
- Caffarri, Stefano; Croce, Roberta; Breton, Jacques
- Journal of Biological Chemistry, Vol. 276, Issue 38
The photoprotective molecular switch in the photosystem II antenna
journal, January 2012
- Ruban, Alexander V.; Johnson, Matthew P.; Duffy, Christopher D. P.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
Singlet Energy Dissipation in the Photosystem II Light-Harvesting Complex Does Not Involve Energy Transfer to Carotenoids
journal, April 2010
- Müller, Marc G.; Lambrev, Petar; Reus, Michael
- ChemPhysChem, Vol. 11, Issue 6
From light-harvesting to photoprotection: structural basis of the dynamic switch of the major antenna complex of plants (LHCII)
journal, October 2015
- Liguori, Nicoletta; Periole, Xavier; Marrink, Siewert J.
- Scientific Reports, Vol. 5, Issue 1
9-cis-Neoxanthin in Light Harvesting Complexes of Photosystem II Regulates the Binding of Violaxanthin and Xanthophyll Cycle
journal, March 2017
- Wang, Ke; Tu, Wenfeng; Liu, Cheng
- Plant Physiology, Vol. 174, Issue 1
The back and forth of energy transfer between carotenoids and chlorophylls and its role in the regulation of light harvesting
journal, April 2013
- Holleboom, Christoph-Peter; Walla, Peter J.
- Photosynthesis Research, Vol. 119, Issue 1-2
LHCII Populations in Different Quenching States Are Present in the Thylakoid Membranes in a Ratio that Depends on the Light Conditions
journal, June 2015
- Tian, Lijin; Dinc, Emine; Croce, Roberta
- The Journal of Physical Chemistry Letters, Vol. 6, Issue 12
Lessons from nature about solar light harvesting
journal, September 2011
- Scholes, Gregory D.; Fleming, Graham R.; Olaya-Castro, Alexandra
- Nature Chemistry, Vol. 3, Issue 10
Carotenoid-to-Chlorophyll Energy Transfer in Recombinant Major Light-Harvesting Complex (LHCII) of Higher Plants. I. Femtosecond Transient Absorption Measurements
journal, February 2001
- Croce, Roberta; Müller, Marc G.; Bassi, Roberto
- Biophysical Journal, Vol. 80, Issue 2
Measuring ultrashort laser pulses in the time-frequency domain using frequency-resolved optical gating
journal, September 1997
- Trebino, Rick; DeLong, Kenneth W.; Fittinghoff, David N.
- Review of Scientific Instruments, Vol. 68, Issue 9, p. 3277-3295
Two lutein molecules in LHCII have different conformations and functions: Insights into the molecular mechanism of thermal dissipation in plants
journal, April 2007
- Yan, Hanchi; Zhang, Pingfeng; Wang, Chao
- Biochemical and Biophysical Research Communications, Vol. 355, Issue 2
Pathways of Energy Flow in LHCII from Two-Dimensional Electronic Spectroscopy
journal, November 2009
- Schlau-Cohen, Gabriela S.; Calhoun, Tessa R.; Ginsberg, Naomi S.
- The Journal of Physical Chemistry B, Vol. 113, Issue 46