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Title: Vibronic mixing enables ultrafast energy flow in light-harvesting complex II

Abstract

Since the discovery of quantum beats in the two-dimensional electronic spectra of photosynthetic pigment-protein complexes over a decade ago, the origin and mechanistic function of these beats in photosynthetic light-harvesting has been extensively debated. The current consensus is that these long-lived oscillatory features likely result from electronic-vibrational mixing, however, it remains uncertain if such mixing significantly influences energy transport. Here, we examine the interplay between the electronic and nuclear degrees of freedom (DoF) during the excitation energy transfer (EET) dynamics of light-harvesting complex II (LHCII) with two-dimensional electronic-vibrational spectroscopy. Particularly, we show the involvement of the nuclear DoF during EET through the participation of higher-lying vibronic chlorophyll states and assign observed oscillatory features to specific EET pathways, demonstrating a significant step in mapping evolution from energy to physical space. These frequencies correspond to known vibrational modes of chlorophyll, suggesting that electronic-vibrational mixing facilitates rapid EET over moderately size energy gaps.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2];  [1]
  1. Univ. of California, Berkeley, CA (United States); Kavli Energy NanoScience Institute, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF)
OSTI Identifier:
1631639
Grant/Contract Number:  
AC02-05CH11231; DGE1752814
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; photochemistry; physical chemistry

Citation Formats

Arsenault, Eric A., Yoneda, Yusuke, Iwai, Masakazu, Niyogi, Krishna K., and Fleming, Graham R. Vibronic mixing enables ultrafast energy flow in light-harvesting complex II. United States: N. p., 2020. Web. https://doi.org/10.1038/s41467-020-14970-1.
Arsenault, Eric A., Yoneda, Yusuke, Iwai, Masakazu, Niyogi, Krishna K., & Fleming, Graham R. Vibronic mixing enables ultrafast energy flow in light-harvesting complex II. United States. https://doi.org/10.1038/s41467-020-14970-1
Arsenault, Eric A., Yoneda, Yusuke, Iwai, Masakazu, Niyogi, Krishna K., and Fleming, Graham R. Thu . "Vibronic mixing enables ultrafast energy flow in light-harvesting complex II". United States. https://doi.org/10.1038/s41467-020-14970-1. https://www.osti.gov/servlets/purl/1631639.
@article{osti_1631639,
title = {Vibronic mixing enables ultrafast energy flow in light-harvesting complex II},
author = {Arsenault, Eric A. and Yoneda, Yusuke and Iwai, Masakazu and Niyogi, Krishna K. and Fleming, Graham R.},
abstractNote = {Since the discovery of quantum beats in the two-dimensional electronic spectra of photosynthetic pigment-protein complexes over a decade ago, the origin and mechanistic function of these beats in photosynthetic light-harvesting has been extensively debated. The current consensus is that these long-lived oscillatory features likely result from electronic-vibrational mixing, however, it remains uncertain if such mixing significantly influences energy transport. Here, we examine the interplay between the electronic and nuclear degrees of freedom (DoF) during the excitation energy transfer (EET) dynamics of light-harvesting complex II (LHCII) with two-dimensional electronic-vibrational spectroscopy. Particularly, we show the involvement of the nuclear DoF during EET through the participation of higher-lying vibronic chlorophyll states and assign observed oscillatory features to specific EET pathways, demonstrating a significant step in mapping evolution from energy to physical space. These frequencies correspond to known vibrational modes of chlorophyll, suggesting that electronic-vibrational mixing facilitates rapid EET over moderately size energy gaps.},
doi = {10.1038/s41467-020-14970-1},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United States},
year = {2020},
month = {3}
}

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Works referenced in this record:

Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature
journal, February 2010

  • Collini, Elisabetta; Wong, Cathy Y.; Wilk, Krystyna E.
  • Nature, Vol. 463, Issue 7281
  • DOI: 10.1038/nature08811

A method for the direct measurement of electronic site populations in a molecular aggregate using two-dimensional electronic-vibrational spectroscopy
journal, September 2015

  • Lewis, Nicholas H. C.; Dong, Hui; Oliver, Thomas A. A.
  • The Journal of Chemical Physics, Vol. 143, Issue 12
  • DOI: 10.1063/1.4931634

Two-color two-dimensional Fourier transform electronic spectroscopy with a pulse-shaper
journal, January 2008

  • Myers, Jeffrey A.; Lewis, Kristin L.; Tekavec, Patrick F.
  • Optics Express, Vol. 16, Issue 22
  • DOI: 10.1364/OE.16.017420

Signatures of vibronic coupling in two-dimensional electronic-vibrational and vibrational-electronic spectroscopies
journal, September 2017

  • Gaynor, James D.; Khalil, Munira
  • The Journal of Chemical Physics, Vol. 147, Issue 9
  • DOI: 10.1063/1.4991745

Vibronic coherence in oxygenic photosynthesis
journal, July 2014

  • Fuller, Franklin D.; Pan, Jie; Gelzinis, Andrius
  • Nature Chemistry, Vol. 6, Issue 8
  • DOI: 10.1038/nchem.2005

Ultrafast energy transfer within the photosystem II core complex
journal, January 2017

  • Pan, Jie; Gelzinis, Andrius; Chorošajev, Vladimir
  • Physical Chemistry Chemical Physics, Vol. 19, Issue 23
  • DOI: 10.1039/C7CP01673E

Quantum oscillatory exciton migration in photosynthetic reaction centers
journal, August 2010

  • Abramavicius, Darius; Mukamel, Shaul
  • The Journal of Chemical Physics, Vol. 133, Issue 6
  • DOI: 10.1063/1.3458824

Observation of Electronic Excitation Transfer Through Light Harvesting Complex II Using Two-Dimensional Electronic–Vibrational Spectroscopy
journal, October 2016

  • Lewis, Nicholas H. C.; Gruenke, Natalie L.; Oliver, Thomas A. A.
  • The Journal of Physical Chemistry Letters, Vol. 7, Issue 20
  • DOI: 10.1021/acs.jpclett.6b02280

Exciton-vibrational resonance and dynamics of charge separation in the photosystem II reaction center
journal, January 2017

  • Novoderezhkin, Vladimir I.; Romero, Elisabet; Prior, Javier
  • Physical Chemistry Chemical Physics, Vol. 19, Issue 7
  • DOI: 10.1039/C6CP07308E

Spectroscopic elucidation of uncoupled transition energies in the major photosynthetic light-harvesting complex, LHCII
journal, July 2010

  • Schlau-Cohen, G. S.; Calhoun, T. R.; Ginsberg, N. S.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 30
  • DOI: 10.1073/pnas.1006230107

Vibrational Beatings Conceal Evidence of Electronic Coherence in the FMO Light-Harvesting Complex
journal, October 2014

  • Tempelaar, Roel; Jansen, Thomas L. C.; Knoester, Jasper
  • The Journal of Physical Chemistry B, Vol. 118, Issue 45
  • DOI: 10.1021/jp510074q

Excitation Dynamics in the LHCII Complex of Higher Plants:  Modeling Based on the 2.72 Å Crystal Structure
journal, May 2005

  • Novoderezhkin, Vladimir I.; Palacios, Miguel A.; van Amerongen, Herbert
  • The Journal of Physical Chemistry B, Vol. 109, Issue 20
  • DOI: 10.1021/jp044082f

Determining the static electronic and vibrational energy correlations via two-dimensional electronic-vibrational spectroscopy
journal, May 2015

  • Dong, Hui; Lewis, Nicholas H. C.; Oliver, Thomas A. A.
  • The Journal of Chemical Physics, Vol. 142, Issue 17
  • DOI: 10.1063/1.4919684

Toward anharmonic computations of vibrational spectra for large molecular systems
journal, August 2011

  • Barone, Vincenzo; Biczysko, Malgorzata; Bloino, Julien
  • International Journal of Quantum Chemistry, Vol. 112, Issue 9
  • DOI: 10.1002/qua.23224

Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems
journal, April 2007

  • Engel, Gregory S.; Calhoun, Tessa R.; Read, Elizabeth L.
  • Nature, Vol. 446, Issue 7137
  • DOI: 10.1038/nature05678

Anti-Correlated Spectral Motion in Bisphthalocyanines:  Evidence for Vibrational Modulation of Electronic Mixing
journal, December 2005

  • Prall, Bradley S.; Parkinson, Dilworth Y.; Ishikawa, Naoto
  • The Journal of Physical Chemistry A, Vol. 109, Issue 48
  • DOI: 10.1021/jp054225d

Energy-Transfer Dynamics in the LHCII Complex of Higher Plants:  Modified Redfield Approach
journal, July 2004

  • Novoderezhkin, Vladimir I.; Palacios, Miguel A.; van Amerongen, Herbert
  • The Journal of Physical Chemistry B, Vol. 108, Issue 29
  • DOI: 10.1021/jp0496001

Treatment of Herzberg-Teller and non-Condon effects in optical spectra with Hierarchical Equations of Motion
journal, November 2018


Light-harvesting complex Lhcb9 confers a green alga-type photosystem I supercomplex to the moss Physcomitrella patens
journal, January 2015


Exciton-vibrational coupling in molecular aggregates: Electronic versus vibronic dimer
journal, February 2012


Measuring correlated electronic and vibrational spectral dynamics using line shapes in two-dimensional electronic-vibrational spectroscopy
journal, May 2015

  • Lewis, Nicholas H. C.; Dong, Hui; Oliver, Thomas A. A.
  • The Journal of Chemical Physics, Vol. 142, Issue 17
  • DOI: 10.1063/1.4919686

Comparison of Electronic and Vibrational Coherence Measured by Two-Dimensional Electronic Spectroscopy
journal, July 2011

  • Turner, Daniel B.; Wilk, Krystyna E.; Curmi, Paul M. G.
  • The Journal of Physical Chemistry Letters, Vol. 2, Issue 15
  • DOI: 10.1021/jz200811p

Direct evidence of quantum transport in photosynthetic light-harvesting complexes
journal, December 2011

  • Panitchayangkoon, G.; Voronine, D. V.; Abramavicius, D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 52
  • DOI: 10.1073/pnas.1105234108

Following Coupled Electronic-Nuclear Motion through Conical Intersections in the Ultrafast Relaxation of β-Apo-8′-carotenal
journal, July 2015

  • Oliver, Thomas A. A.; Fleming, Graham R.
  • The Journal of Physical Chemistry B, Vol. 119, Issue 34
  • DOI: 10.1021/acs.jpcb.5b04893

Direct observation of energy transfer in a photosynthetic membrane: chlorophyll b to chlorophyll a transfer in LHC
journal, December 1989

  • Eads, Daniel D.; Castner, Edward W.; Alberte, Randall S.
  • The Journal of Physical Chemistry, Vol. 93, Issue 26
  • DOI: 10.1021/j100363a001

Correlating the motion of electrons and nuclei with two-dimensional electronic-vibrational spectroscopy
journal, June 2014

  • Oliver, T. A. A.; Lewis, N. H. C.; Fleming, G. R.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 28
  • DOI: 10.1073/pnas.1409207111

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

Smoothing and Differentiation of Data by Simplified Least Squares Procedures.
journal, July 1964

  • Savitzky, Abraham.; Golay, M. J. E.
  • Analytical Chemistry, Vol. 36, Issue 8
  • DOI: 10.1021/ac60214a047

Vibronic phenomena and exciton–vibrational interference in two-dimensional spectra of molecular aggregates
journal, January 2014

  • Butkus, Vytautas; Valkunas, Leonas; Abramavicius, Darius
  • The Journal of Chemical Physics, Vol. 140, Issue 3
  • DOI: 10.1063/1.4861466

Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield–Förster picture
journal, January 2011

  • Novoderezhkin, Vladimir; Marin, Alessandro; van Grondelle, Rienk
  • Physical Chemistry Chemical Physics, Vol. 13, Issue 38
  • DOI: 10.1039/c1cp21079c

Two-Dimensional Electronic-Vibrational Spectroscopy of Chlorophyll a and b
journal, February 2016

  • Lewis, Nicholas H. C.; Fleming, Graham R.
  • The Journal of Physical Chemistry Letters, Vol. 7, Issue 5
  • DOI: 10.1021/acs.jpclett.6b00037

Vibronic origin of long-lived coherence in an artificial molecular light harvester
journal, July 2015

  • Lim, James; Paleček, David; Caycedo-Soler, Felipe
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms8755

Correlated Protein Environments Drive Quantum Coherence Lifetimes in Photosynthetic Pigment-Protein Complexes
journal, January 2018


Mapping Vibronic Couplings in a Solar Cell Dye with Polarization-Selective Two-Dimensional Electronic–Vibrational Spectroscopy
journal, October 2018

  • Gaynor, James D.; Petrone, Alessio; Li, Xiaosong
  • The Journal of Physical Chemistry Letters, Vol. 9, Issue 21
  • DOI: 10.1021/acs.jpclett.8b02752

Quantum Coherence Enabled Determination of the Energy Landscape in Light-Harvesting Complex II
journal, December 2009

  • Calhoun, Tessa R.; Ginsberg, Naomi S.; Schlau-Cohen, Gabriela S.
  • The Journal of Physical Chemistry B, Vol. 113, Issue 51
  • DOI: 10.1021/jp908300c

Identification and characterization of diverse coherences in the Fenna–Matthews–Olson complex
journal, May 2018

  • Thyrhaug, Erling; Tempelaar, Roel; Alcocer, Marcelo J. P.
  • Nature Chemistry, Vol. 10, Issue 7
  • DOI: 10.1038/s41557-018-0060-5

Coherent Picosecond Exciton Dynamics in a Photosynthetic Reaction Center
journal, October 2012

  • Westenhoff, Sebastian; Palec̆ek, David; Edlund, Petra
  • Journal of the American Chemical Society, Vol. 134, Issue 40
  • DOI: 10.1021/ja3065478

Origin of long-lived oscillations in 2D-spectra of a quantum vibronic model: Electronic versus vibrational coherence
journal, December 2013

  • Plenio, M. B.; Almeida, J.; Huelga, S. F.
  • The Journal of Chemical Physics, Vol. 139, Issue 23
  • DOI: 10.1063/1.4846275

Two-Dimensional Electronic–Vibrational Spectroscopy of Coupled Molecular Complexes: A Near-Analytical Approach
journal, April 2019

  • Bhattacharyya, Pallavi; Fleming, Graham R.
  • The Journal of Physical Chemistry Letters, Vol. 10, Issue 9
  • DOI: 10.1021/acs.jpclett.9b00588

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

Vibrational Coherence Transfer and Trapping as Sources for Long-Lived Quantum Beats in Polarized Emission from Energy Transfer Complexes
journal, December 2004

  • Cina, Jeffrey A.; Fleming, Graham R.
  • The Journal of Physical Chemistry A, Vol. 108, Issue 51
  • DOI: 10.1021/jp047015u

Phase-cycling schemes for pump–probe beam geometry two-dimensional electronic spectroscopy
journal, October 2012


Effects of Herzberg–Teller vibronic coupling on coherent excitation energy transfer
journal, November 2016

  • Zhang, Hou-Dao; Qiao, Qin; Xu, Rui-Xue
  • The Journal of Chemical Physics, Vol. 145, Issue 20
  • DOI: 10.1063/1.4968031

Vibronic Coherence in the Charge Separation Process of the Rhodobacter sphaeroides Reaction Center
journal, March 2018

  • Ma, Fei; Romero, Elisabet; Jones, Michael R.
  • The Journal of Physical Chemistry Letters, Vol. 9, Issue 8
  • DOI: 10.1021/acs.jpclett.8b00108

Resolving molecular vibronic structure using high-sensitivity two-dimensional electronic spectroscopy
journal, October 2015

  • Bizimana, Laurie A.; Brazard, Johanna; Carbery, William P.
  • The Journal of Chemical Physics, Vol. 143, Issue 16
  • DOI: 10.1063/1.4934717

Elucidation of near-resonance vibronic coherence lifetimes by nonadiabatic electronic-vibrational state character mixing
journal, August 2018

  • Yeh, Shu-Hao; Hoehn, Ross D.; Allodi, Marco A.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 37
  • DOI: 10.1073/pnas.1701390115

The molecular organisation of the photosynthetic membranes of higher plants
journal, June 1986


Elucidation of the timescales and origins of quantum electronic coherence in LHCII
journal, March 2012

  • Schlau-Cohen, Gabriela S.; Ishizaki, Akihito; Calhoun, Tessa R.
  • Nature Chemistry, Vol. 4, Issue 5
  • DOI: 10.1038/nchem.1303

Vibronic Enhancement of Algae Light Harvesting
journal, December 2016


Simulations of the temperature dependence of energy transfer in the PSI core antenna
journal, July 1992


Two-dimensional electronic-vibrational spectroscopic study of conical intersection dynamics: an experimental and electronic structure study
journal, January 2019

  • Wu, Eric C.; Ge, Qinghui; Arsenault, Eric A.
  • Physical Chemistry Chemical Physics, Vol. 21, Issue 26
  • DOI: 10.1039/C8CP05264F

Origin of Long-Lived Coherences in Light-Harvesting Complexes
journal, June 2012

  • Christensson, Niklas; Kauffmann, Harald F.; Pullerits, Tõnu
  • The Journal of Physical Chemistry B, Vol. 116, Issue 25
  • DOI: 10.1021/jp304649c

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