skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: 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.

Authors:
ORCiD logo; ; ; ORCiD logo; ORCiD logo
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. https://doi.org/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 = {2020},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1038/s41467-020-15074-6

Citation Metrics:
Cited by: 3 works
Citation information provided by
Web of Science

Save / Share:

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
  • DOI: 10.1039/c003389h

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
  • DOI: 10.1074/jbc.M114.607770

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
  • DOI: 10.1021/jacs.8b04844

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
  • DOI: 10.1021/acs.jpclett.7b02486

Control of the light harvesting function of chloroplast membranes: The LHCII-aggregation model for non-photochemical quenching
journal, July 2005


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
  • DOI: 10.1021/jp001752i

Capturing the Quenching Mechanism of Light-Harvesting Complexes of Plants by Zooming in on the Ensemble
journal, November 2019


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
  • DOI: 10.1007/s11120-018-0607-8

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
  • DOI: 10.1007/BF02183041

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
  • DOI: 10.1021/bi010342x

Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants
journal, October 2017


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
  • DOI: 10.1021/bi062031y

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
  • DOI: 10.1073/pnas.0736959100

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
  • DOI: 10.1016/j.bbamem.2016.10.010

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
  • DOI: 10.1021/acs.jpclett.5b00034

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
  • DOI: 10.1039/C5CP01905B

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
  • DOI: 10.1039/C4CP00876F

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
  • DOI: 10.1021/jp070573z

Linear dichroism and circular dichroism in photosynthesis research
journal, May 2009


The Electronic Structure of Lutein 2 Is Optimized for Light Harvesting in Plants
journal, March 2019


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
  • DOI: 10.1021/acs.jpclett.7b03049

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
  • DOI: 10.1016/j.bpj.2010.03.028

Far-red fluorescence: A direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching
journal, October 2008


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
  • DOI: 10.1016/j.bpj.2011.09.055

Carotenoid-Bacteriochlorophyll Energy Transfer in LH2 Complexes Studied with 10-fs Time Resolution
journal, April 2006


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
  • DOI: 10.1021/cr020674n

Ultrafast excited state relaxation in long-chain polyenes
journal, July 2010


Zwischenmolekulare Energiewanderung und Fluoreszenz
journal, January 1948


Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting
journal, January 2005


Different carotenoid conformations have distinct functions in light-harvesting regulation in plants
journal, December 2017


Nanodiscs in Membrane Biochemistry and Biophysics
journal, February 2017


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
  • DOI: 10.1038/nature02373

Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein
journal, May 2008


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
  • DOI: 10.1074/jbc.274.47.33510

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
  • DOI: 10.1073/pnas.1205561110

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
  • DOI: 10.1073/pnas.1105411108

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
  • DOI: 10.1073/pnas.0903536106

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
  • DOI: 10.1038/nchembio.1755

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
  • DOI: 10.1038/emboj.2008.276

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
  • DOI: 10.1364/OE.25.018950

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
  • DOI: 10.1021/acs.jpcb.9b06293

The carotenoid pathway: what is important for excitation quenching in plant antenna complexes?
journal, January 2017

  • Fox, Kieran F.; Balevičius, Vytautas; Chmeliov, Jevgenij
  • Physical Chemistry Chemical Physics, Vol. 19, Issue 34
  • DOI: 10.1039/C7CP03535G

Effect of xanthophyll composition on the chlorophyll excited state lifetime in plant leaves and isolated LHCII
journal, July 2010


Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis
journal, June 2013


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
  • DOI: 10.1038/nature06262

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
  • DOI: 10.1039/C7SC04814A

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
  • DOI: 10.1021/acs.jpcb.5b05592

Theoretical study of vibrational relaxation and internal conversion dynamics of chlorophyll-a in ethyl acetate solvent in femtosecond laser fields
journal, December 2006


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
  • DOI: 10.1038/nature03795

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
  • DOI: 10.1038/nplants.2016.45

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
  • DOI: 10.1021/jp1034163

From isolated light-harvesting complexes to the thylakoid membrane: a single-molecule perspective
journal, January 2018


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
  • DOI: 10.1021/jp066458q

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
  • DOI: 10.1074/jbc.M105199200

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
  • DOI: 10.1016/j.bbabio.2011.04.007

Singlet Energy Dissipation in the Photosystem II Light-Harvesting Complex Does Not Involve Energy Transfer to Carotenoids
journal, April 2010


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
  • DOI: 10.1038/srep15661

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
  • DOI: 10.1104/pp.17.00029

The back and forth of energy transfer between carotenoids and chlorophylls and its role in the regulation of light harvesting
journal, April 2013


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
  • DOI: 10.1021/acs.jpclett.5b00944

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
  • DOI: 10.1038/nchem.1145

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
  • DOI: 10.1063/1.1148286

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
  • DOI: 10.1016/j.bbrc.2007.01.172

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
  • DOI: 10.1021/jp9066586