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

Journal Article · · Nature Communications

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.

Research Organization:
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
SC0018097
OSTI ID:
1619554
Journal Information:
Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 11; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (70)

Molecular Mechanisms of Photosynthesis book December 2002
Zwischenmolekulare Energiewanderung und Fluoreszenz journal January 1948
Singlet Energy Dissipation in the Photosystem II Light-Harvesting Complex Does Not Involve Energy Transfer to Carotenoids journal April 2010
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria book January 2014
Photophysics of the carotenoids associated with the xanthophyll cycle in photosynthesis journal September 1994
Linear dichroism and circular dichroism in photosynthesis research journal May 2009
The back and forth of energy transfer between carotenoids and chlorophylls and its role in the regulation of light harvesting journal April 2013
Time-resolved fluorescence measurements on leaves: principles and recent developments journal November 2018
Carotenoid-to-Chlorophyll Energy Transfer in Recombinant Major Light-Harvesting Complex (LHCII) of Higher Plants. I. Femtosecond Transient Absorption Measurements journal February 2001
Reconstitution of Membrane Proteins in Phospholipid Bilayer Nanodiscs book January 2009
The photoprotective molecular switch in the photosystem II antenna journal January 2012
Disentangling protein and lipid interactions that control a molecular switch in photosynthetic light harvesting journal January 2017
Two lutein molecules in LHCII have different conformations and functions: Insights into the molecular mechanism of thermal dissipation in plants journal April 2007
Fluorescence Spectral Dynamics of Single LHCII Trimers journal June 2010
Assembly of the Major Light-Harvesting Complex II in Lipid Nanodiscs journal November 2011
Effect of xanthophyll composition on the chlorophyll excited state lifetime in plant leaves and isolated LHCII journal July 2010
Ultrafast excited state relaxation in long-chain polyenes journal July 2010
The Electronic Structure of Lutein 2 Is Optimized for Light Harvesting in Plants journal March 2019
Capturing the Quenching Mechanism of Light-Harvesting Complexes of Plants by Zooming in on the Ensemble journal November 2019
Theoretical study of vibrational relaxation and internal conversion dynamics of chlorophyll-a in ethyl acetate solvent in femtosecond laser fields journal December 2006
Control of the light harvesting function of chloroplast membranes: The LHCII-aggregation model for non-photochemical quenching journal July 2005
Far-red fluorescence: A direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching journal October 2008
Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis journal June 2013
Nanodiscs in Membrane Biochemistry and Biophysics journal February 2017
Two-Dimensional Electronic Spectroscopy of Light-Harvesting Complex II at Ambient Temperature: A Joint Experimental and Theoretical Study journal August 2015
Spectroscopic Properties of Violaxanthin and Lutein Triplet States in LHCII are Independent of Carotenoid Composition journal October 2019
Single-Molecule Identification of Quenched and Unquenched States of LHCII journal February 2015
LHCII Populations in Different Quenching States Are Present in the Thylakoid Membranes in a Ratio that Depends on the Light Conditions journal June 2015
Snapshot Transient Absorption Spectroscopy of Carotenoid Radical Cations in High-Light-Acclimating Thylakoid Membranes journal November 2017
Revisiting the Role of Xanthophylls in Nonphotochemical Quenching journal January 2018
Time-Resolved Fluorescence Analysis of the Photosystem II Antenna Proteins in Detergent Micelles and Liposomes journal October 2001
Understanding the Changes in the Circular Dichroism of Light Harvesting Complex II upon Varying Its Pigment Composition and Organization journal April 2007
Ultrafast Dynamics of Carotenoid Excited States−From Solution to Natural and Artificial Systems journal April 2004
Chlorophyll-Carotenoid Excitation Energy Transfer in High-Light-Exposed Thylakoid Membranes Investigated by Snapshot Transient Absorption Spectroscopy journal September 2018
Identifying the Pathways of Energy Transfer between Carotenoids and Chlorophylls in LHCII and CP29. A Multicolor, Femtosecond Pump−Probe Study journal October 2000
Carotenoid Radical Cations as a Probe for the Molecular Mechanism of Nonphotochemical Quenching in Oxygenic Photosynthesis journal April 2007
Equilibrium between Quenched and Nonquenched Conformations of the Major Plant Light-Harvesting Complex Studied with High-Pressure Time-Resolved Fluorescence journal July 2007
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
Pathways of Energy Flow in LHCII from Two-Dimensional Electronic Spectroscopy journal November 2009
Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state journal January 2009
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution journal March 2004
Molecular basis of photoprotection and control of photosynthetic light-harvesting journal July 2005
Identification of a mechanism of photoprotective energy dissipation in higher plants journal November 2007
Lessons from nature about solar light harvesting journal September 2011
Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection journal July 2017
Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins journal February 2015
The nature of self-regulation in photosynthetic light-harvesting antenna journal April 2016
Different carotenoid conformations have distinct functions in light-harvesting regulation in plants journal December 2017
Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants journal October 2017
From light-harvesting to photoprotection: structural basis of the dynamic switch of the major antenna complex of plants (LHCII) journal October 2015
Pathways of energy transfer in LHCII revealed by room-temperature 2D electronic spectroscopy journal January 2014
An ‘all pigment’ model of excitation quenching in LHCII journal January 2015
The carotenoid pathway: what is important for excitation quenching in plant antenna complexes? journal January 2017
Impact of the lipid bilayer on energy transfer kinetics in the photosynthetic protein LH2 journal January 2018
Quantum coherence and its interplay with protein environments in photosynthetic electronic energy transfer journal January 2010
Measuring ultrashort laser pulses in the time-frequency domain using frequency-resolved optical gating journal September 1997
Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting journal April 2003
On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls journal July 2009
Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes journal August 2011
Direct interaction of the major light-harvesting complex II and PsbS in nonphotochemical quenching journal March 2013
Chlorophyll Binding to Monomeric Light-harvesting Complex: A MUTATION ANALYSIS OF CHROMOPHORE-BINDING RESIDUES journal November 1999
The Major Antenna Complex of Photosystem II Has a Xanthophyll Binding Site Not Involved in Light Harvesting journal July 2001
Photoprotective Energy Dissipation in Higher Plants Involves Alteration of the Excited State Energy of the Emitting Chlorophyll(s) in the Light Harvesting Antenna II (LHCII) journal June 2009
Pigment Interactions in Light-harvesting Complex II in Different Molecular Environments journal December 2014
9-cis-Neoxanthin in Light Harvesting Complexes of Photosystem II Regulates the Binding of Violaxanthin and Xanthophyll Cycle journal March 2017
Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting journal January 2005
Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein journal May 2008
Ultrabroadband 2D electronic spectroscopy with high-speed, shot-to-shot detection journal January 2017
From isolated light-harvesting complexes to the thylakoid membrane: a single-molecule perspective journal January 2018
Carotenoid-Bacteriochlorophyll Energy Transfer in LH2 Complexes Studied with 10-fs Time Resolution journal April 2006