Observation of Electronic Excitation Transfer Through Light Harvesting Complex II Using Two-Dimensional Electronic-Vibrational Spectroscopy

Lewis, Nicholas H.  C.; Gruenke, Natalie L.; Oliver, Thomas A.  A.; Ballottari, Matteo; Bassi, Roberto; Fleming, Graham R.

doi:10.1021/acs.jpclett.6b02280

Title: Observation of Electronic Excitation Transfer Through Light Harvesting Complex II Using Two-Dimensional Electronic-Vibrational Spectroscopy

Journal Article · Wed Oct 05 00:00:00 EDT 2016 · Journal of Physical Chemistry Letters

DOI:https://doi.org/10.1021/acs.jpclett.6b02280· OSTI ID:1378344

Lewis, Nicholas H. C. ^[1]; Gruenke, Natalie L. ^[1]; Oliver, Thomas A. A. ^[1]; Ballottari, Matteo ^[2]; Bassi, Roberto ^[2]; Fleming, Graham R. ^[1]

Univ. of California, Berkeley, CA (United States). Dept. of Chemistry; ; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division; Kavli Energy nanoscience Inst. at Berkeley, CA (United States)
Univ. di Verona (Italy). Dipartimento di Biotecnologie

Light-harvesting complex II (LHCII) serves a central role in light harvesting for oxygenic photosynthesis and is arguably the most important photosynthetic antenna complex. In this article, we present two-dimensional electronic–vibrational (2DEV) spectra of LHCII isolated from spinach, demonstrating the possibility of using this technique to track the transfer of electronic excitation energy between specific pigments within the complex. We assign the spectral bands via comparison with the 2DEV spectra of the isolated chromophores, chlorophyll a and b, and present evidence that excitation energy between the pigments of the complex are observed in these spectra. Lastly, we analyze the essential components of the 2DEV spectra using singular value decomposition, which makes it possible to reveal the relaxation pathways within this complex.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231; AC03-76F000098; SOLENALGAE nr 679814

OSTI ID:: 1378344

Journal Information:: Journal of Physical Chemistry Letters, Vol. 7, Issue 20; ISSN 1948-7185

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 41 works

Citation information provided by
Web of Science

References (53)

Molecular Mechanisms of Photosynthesis Blankenship, Robert E. https://doi.org/10.1002/9780470758472	book	December 2002
Chapter 8. Structure and Function of Photosystem II Light-Harvesting Proteins (Lhcb) of Higher Plants van Amerongen, Herbert; Croce, Roberta Primary Processes of Photosynthesis, Part 1 https://doi.org/10.1039/9781847558152-00329	book	January 2007
Carotenoids in Photosynthesis Frank, Harry A.; Cogdell, Richard J. Photochemistry and Photobiology, Vol. 63, Issue 3 https://doi.org/10.1111/j.1751-1097.1996.tb03022.x	journal	March 1996
Two-Photon Excitation Spectrum of Light-Harvesting Complex II and Fluorescence Upconversion after One- and Two-Photon Excitation of the Carotenoids Walla, Peter J.; Yom, Jenny; Krueger, Brent P. The Journal of Physical Chemistry B, Vol. 104, Issue 19 https://doi.org/10.1021/jp9943023	journal	April 2000
Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting Holt, N. E. Science, Vol. 307, Issue 5708 https://doi.org/10.1126/science.1105833	journal	January 2005
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
Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein Ahn, T. K.; Avenson, T. J.; Ballottari, M. Science, Vol. 320, Issue 5877 https://doi.org/10.1126/science.1154800	journal	May 2008
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
Role of Xanthophylls in Light Harvesting in Green Plants: A Spectroscopic Investigation of Mutant LHCII and Lhcb Pigment–Protein Complexes Fuciman, Marcel; Enriquez, Miriam M.; Polívka, Tomáš The Journal of Physical Chemistry B, Vol. 116, Issue 12 https://doi.org/10.1021/jp210042z	journal	March 2012
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
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield–Förster picture Novoderezhkin, Vladimir; Marin, Alessandro; van Grondelle, Rienk Physical Chemistry Chemical Physics, Vol. 13, Issue 38 https://doi.org/10.1039/c1cp21079c	journal	January 2011
Atomic model of plant light-harvesting complex by electron crystallography Kühlbrandt, Werner; Wang, Da Neng; Fujiyoshi, Yoshinori Nature, Vol. 367, Issue 6464 https://doi.org/10.1038/367614a0	journal	February 1994
Chlorophyll Binding to Monomeric Light-harvesting Complex: A MUTATION ANALYSIS OF CHROMOPHORE-BINDING RESIDUES Remelli, Rosaria; Varotto, Claudio; Sandonà, Dorianna Journal of Biological Chemistry, Vol. 274, Issue 47 https://doi.org/10.1074/jbc.274.47.33510	journal	November 1999
Carotenoid-binding Sites of the Major Light-harvesting Complex II of Higher Plants Croce, Roberta; Weiss, Saskia; Bassi, Roberto Journal of Biological Chemistry, Vol. 274, Issue 42 https://doi.org/10.1074/jbc.274.42.29613	journal	October 1999
Energy transfer in photosynthesis: experimental insights and quantitative models van Grondelle, Rienk; Novoderezhkin, Vladimir I. Phys. Chem. Chem. Phys., Vol. 8, Issue 7 https://doi.org/10.1039/B514032C	journal	January 2006
Direct observation of energy transfer in a photosynthetic membrane: chlorophyll b to chlorophyll a transfer in LHC Eads, Daniel D.; Castner, Edward W.; Alberte, Randall S. The Journal of Physical Chemistry, Vol. 93, Issue 26 https://doi.org/10.1021/j100363a001	journal	December 1989
Spectroscopic properties of LHC-II, the main light-harvesting chlorophyll a/b protein complex from chloroplast membranes Hemelrijk, Petra W.; Kwa, Stefan L. S.; van Grondelle, Rienk Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1098, Issue 2 https://doi.org/10.1016/S0005-2728(05)80331-7	journal	January 1992
Direct Observation of Ultrafast Energy-Transfer Processes in Light Harvesting Complex II Du, Mei; Xie, Xiaoliang; Mets, Laurens The Journal of Physical Chemistry, Vol. 98, Issue 17 https://doi.org/10.1021/j100068a041	journal	April 1994
Ultrafast Excitation Energy Transfer and Exciton-Exciton Annihilation Processes in Isolated Light Harvesting Complexes of Photosystem II (LHC II) from Spinach Bittner, Thomas; Irrgang, Klaus-Dieter; Renger, Gernot The Journal of Physical Chemistry, Vol. 98, Issue 46 https://doi.org/10.1021/j100097a004	journal	November 1994
Ultrafast Energy Transfer in LHC-II Revealed by Three-Pulse Photon Echo Peak Shift Measurements Agarwal, Ritesh; Krueger, Brent P.; Scholes, Gregory D. The Journal of Physical Chemistry B, Vol. 104, Issue 13 https://doi.org/10.1021/jp9915578	journal	April 2000
Single Molecule Spectroscopy on the Light-Harvesting Complex II of Higher Plants Tietz, Carsten; Jelezko, Fedor; Gerken, Uwe Biophysical Journal, Vol. 81, Issue 1 https://doi.org/10.1016/S0006-3495(01)75722-0	journal	July 2001
Chromophore−Chromophore and Chromophore−Protein Interactions in Monomeric Light-Harvesting Complex II of Green Plants Studied by Spectral Hole Burning and Fluorescence Line Narrowing Pieper, Jörg; Rätsep, Margus; Irrgang, Klaus-Dieter The Journal of Physical Chemistry B, Vol. 113, Issue 31 https://doi.org/10.1021/jp900836p	journal	August 2009
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
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
Quantum Coherence Enabled Determination of the Energy Landscape in Light-Harvesting Complex II Calhoun, Tessa R.; Ginsberg, Naomi S.; Schlau-Cohen, Gabriela S. The Journal of Physical Chemistry B, Vol. 113, Issue 51 https://doi.org/10.1021/jp908300c	journal	December 2009
Spectroscopic elucidation of uncoupled transition energies in the major photosynthetic light-harvesting complex, LHCII Schlau-Cohen, G. S.; Calhoun, T. R.; Ginsberg, N. S. Proceedings of the National Academy of Sciences, Vol. 107, Issue 30 https://doi.org/10.1073/pnas.1006230107	journal	July 2010
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
How Proteins Trigger Excitation Energy Transfer in the FMO Complex of Green Sulfur Bacteria Adolphs, Julia; Renger, Thomas Biophysical Journal, Vol. 91, Issue 8 https://doi.org/10.1529/biophysj.105.079483	journal	October 2006
Atomistic Study of the Long-Lived Quantum Coherences in the Fenna-Matthews-Olson Complex Shim, Sangwoo; Rebentrost, Patrick; Valleau, Stéphanie Biophysical Journal, Vol. 102, Issue 3 https://doi.org/10.1016/j.bpj.2011.12.021	journal	February 2012
Theoretical Study on Excited States of Bacteriochlorophyll a in Solutions with Density Functional Assessment Higashi, Masahiro; Kosugi, Takahiro; Hayashi, Shigehiko The Journal of Physical Chemistry B, Vol. 118, Issue 37 https://doi.org/10.1021/jp507259g	journal	September 2014
Ab Initio Nonadiabatic Dynamics of Multichromophore Complexes: A Scalable Graphical-Processing-Unit-Accelerated Exciton Framework Sisto, Aaron; Glowacki, David R.; Martinez, Todd J. Accounts of Chemical Research, Vol. 47, Issue 9 https://doi.org/10.1021/ar500229p	journal	July 2014
Influence of Force Fields and Quantum Chemistry Approach on Spectral Densities of BChl a in Solution and in FMO Proteins Chandrasekaran, Suryanarayanan; Aghtar, Mortaza; Valleau, Stéphanie The Journal of Physical Chemistry B, Vol. 119, Issue 31 https://doi.org/10.1021/acs.jpcb.5b03654	journal	July 2015
Quantum Chemical Studies of Light Harvesting Curutchet, Carles; Mennucci, Benedetta Chemical Reviews, Vol. 117, Issue 2 https://doi.org/10.1021/acs.chemrev.5b00700	journal	March 2016
Unified treatment of quantum coherent and incoherent hopping dynamics in electronic energy transfer: Reduced hierarchy equation approach Ishizaki, Akihito; Fleming, Graham R. The Journal of Chemical Physics, Vol. 130, Issue 23 https://doi.org/10.1063/1.3155372	journal	June 2009
Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature Ishizaki, A.; Fleming, G. R. Proceedings of the National Academy of Sciences, Vol. 106, Issue 41 https://doi.org/10.1073/pnas.0908989106	journal	October 2009
An efficient method to calculate excitation energy transfer in light-harvesting systems: application to the Fenna–Matthews–Olson complex Ritschel, Gerhard; Roden, Jan; Strunz, Walter T. New Journal of Physics, Vol. 13, Issue 11 https://doi.org/10.1088/1367-2630/13/11/113034	journal	November 2011
A Structure-Based Model of Energy Transfer Reveals the Principles of Light Harvesting in Photosystem II Supercomplexes Bennett, Doran I. G.; Amarnath, Kapil; Fleming, Graham R. Journal of the American Chemical Society, Vol. 135, Issue 24 https://doi.org/10.1021/ja403685a	journal	June 2013
Correlating the motion of electrons and nuclei with two-dimensional electronic-vibrational spectroscopy Oliver, T. A. A.; Lewis, N. H. C.; Fleming, G. R. Proceedings of the National Academy of Sciences, Vol. 111, Issue 28 https://doi.org/10.1073/pnas.1409207111	journal	June 2014
A method for the direct measurement of electronic site populations in a molecular aggregate using two-dimensional electronic-vibrational spectroscopy Lewis, Nicholas H. C.; Dong, Hui; Oliver, Thomas A. A. The Journal of Chemical Physics, Vol. 143, Issue 12 https://doi.org/10.1063/1.4931634	journal	September 2015
Determining the static electronic and vibrational energy correlations via two-dimensional electronic-vibrational spectroscopy Dong, Hui; Lewis, Nicholas H. C.; Oliver, Thomas A. A. The Journal of Chemical Physics, Vol. 142, Issue 17 https://doi.org/10.1063/1.4919684	journal	May 2015
Measuring correlated electronic and vibrational spectral dynamics using line shapes in two-dimensional electronic-vibrational spectroscopy Lewis, Nicholas H. C.; Dong, Hui; Oliver, Thomas A. A. The Journal of Chemical Physics, Vol. 142, Issue 17 https://doi.org/10.1063/1.4919686	journal	May 2015
A Femtosecond Visible/Visible and Visible/Mid-Infrared Transient Absorption Study of the Light Harvesting Complex II Stahl, Andreas D.; Di Donato, Mariangela; van Stokkum, Ivo Biophysical Journal, Vol. 97, Issue 12 https://doi.org/10.1016/j.bpj.2009.09.037	journal	December 2009
Two-Dimensional Electronic-Vibrational Spectroscopy of Chlorophyll a and b Lewis, Nicholas H. C.; Fleming, Graham R. The Journal of Physical Chemistry Letters, Vol. 7, Issue 5 https://doi.org/10.1021/acs.jpclett.6b00037	journal	February 2016
Assignment of the Q-Bands of the Chlorophylls: Coherence Loss via Qx − Qy Mixing Reimers, Jeffrey R.; Cai, Zheng-Li; Kobayashi, Rika Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep02761	journal	September 2013
The infrared absorption of amino acid side chains Barth, Andreas Progress in Biophysics and Molecular Biology, Vol. 74, Issue 3-5 https://doi.org/10.1016/S0079-6107(00)00021-3	journal	January 2000
Vibrational Stark Spectroscopy in Proteins: A Probe and Calibration for Electrostatic Fields Park, Eun Sun; Andrews, Steven S.; Hu, Robert B. The Journal of Physical Chemistry B, Vol. 103, Issue 45 https://doi.org/10.1021/jp992329g	journal	November 1999
Vibrational solvatochromism and electrochromism: Coarse-grained models and their relationships Cho, Minhaeng The Journal of Chemical Physics, Vol. 130, Issue 9 https://doi.org/10.1063/1.3079609	journal	March 2009
Vibrational solvatochromism and electrochromism of infrared probe molecules containing C≡O, C≡N, C=O, or C−F vibrational chromophore Choi, Jun-Ho; Cho, Minhaeng The Journal of Chemical Physics, Vol. 134, Issue 15 https://doi.org/10.1063/1.3580776	journal	April 2011
Titration of individual components in a mixture with resolution of difference spectra, pKs, and redox transitions Shrager, Richard I.; Hendler, Richard W. Analytical Chemistry, Vol. 54, Issue 7 https://doi.org/10.1021/ac00244a031	journal	June 1982
Deconvolutions based on singular value decomposition and the pseudoinverse: a guide for beginners Hendler, Richard W.; Shrager, Richard I. Journal of Biochemical and Biophysical Methods, Vol. 28, Issue 1 https://doi.org/10.1016/0165-022X(94)90061-2	journal	January 1994
Two-color two-dimensional Fourier transform electronic spectroscopy with a pulse-shaper Myers, Jeffrey A.; Lewis, Kristin L.; Tekavec, Patrick F. Optics Express, Vol. 16, Issue 22 https://doi.org/10.1364/OE.16.017420	journal	January 2008
Phase-cycling schemes for pump–probe beam geometry two-dimensional electronic spectroscopy Zhang, Zhengyang; Wells, Kym Lewis; Hyland, Edward William James Chemical Physics Letters, Vol. 550 https://doi.org/10.1016/j.cplett.2012.08.037	journal	October 2012

Cited By (2)

Vibronic mixing enables ultrafast energy flow in light-harvesting complex II Arsenault, Eric A.; Yoneda, Yusuke; Iwai, Masakazu Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14970-1	journal	March 2020
Concentration Effect on Quenching of Chlorophyll a Fluorescence by All-Trans-β-Carotene in Photosynthesis Chen, Chen; Gong, Nan; Li, Zuowei Molecules, Vol. 22, Issue 10 https://doi.org/10.3390/molecules22101585	journal	September 2017

Similar Records

PS2013 Satellite Workshop on Photosynthetic Light-Harvesting Systems

Technical Report · Sat Feb 07 00:00:00 EST 2015 · OSTI ID:1378344

Niederman, Robert A.; Blankenship, Robert E.; Frank, Harry A.

Single-photon absorption by single photosynthetic light-harvesting complexes

Journal Article · Mon Feb 12 00:00:00 EST 2018 · Journal of Physics. B, Atomic, Molecular and Optical Physics · OSTI ID:1378344

Chan, Herman C. H.; Gamel, Omar E.; Fleming, Graham R.; +1 more

Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants

Journal Article · Tue Oct 24 00:00:00 EDT 2017 · Scientific Reports · OSTI ID:1378344

Balevičius, Vytautas; Fox, Kieran F.; Bricker, William P.; +4 more

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND TECHNOLOGY

Title: Observation of Electronic Excitation Transfer Through Light Harvesting Complex II Using Two-Dimensional Electronic-Vibrational Spectroscopy

Citation Formats

References (53)

Cited By (2)

Similar Records

Related Subjects