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

Arsenault, Eric A.; Yoneda, Yusuke; Iwai, Masakazu; Niyogi, Krishna K.; Fleming, Graham R.

doi:10.1038/s41467-020-14970-1

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

Journal Article · 19 March 2020 · Nature Communications

DOI: https://doi.org/10.1038/s41467-020-14970-1 · OSTI ID:1631639

^[1];

^[2];

^[2]; Fleming, Graham R. ^[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)
Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

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.

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Science Foundation (NSF)

Grant/Contract Number:: AC02-05CH11231; DGE1752814

OSTI ID:: 1631639

Journal Information:: Nature Communications, Vol. 11, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 53 works

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Excitation Dynamics in the LHCII Complex of Higher Plants: Modeling Based on the 2.72 Å Crystal Structure Novoderezhkin, Vladimir I.; Palacios, Miguel A.; van Amerongen, Herbert The Journal of Physical Chemistry B, Vol. 109, Issue 20 https://doi.org/10.1021/jp044082f	journal	May 2005
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Vibrational Beatings Conceal Evidence of Electronic Coherence in the FMO Light-Harvesting Complex Tempelaar, Roel; Jansen, Thomas L. C.; Knoester, Jasper The Journal of Physical Chemistry B, Vol. 118, Issue 45 https://doi.org/10.1021/jp510074q	journal	October 2014
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
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Vibronic coherence in oxygenic photosynthesis Fuller, Franklin D.; Pan, Jie; Gelzinis, Andrius Nature Chemistry, Vol. 6, Issue 8 https://doi.org/10.1038/nchem.2005	journal	July 2014
Light-harvesting complex Lhcb9 confers a green alga-type photosystem I supercomplex to the moss Physcomitrella patens Iwai, Masakazu; Yokono, Makio; Kono, Masaru Nature Plants, Vol. 1, Issue 2 https://doi.org/10.1038/nplants.2014.8	journal	January 2015
Identification and characterization of diverse coherences in the Fenna–Matthews–Olson complex Thyrhaug, Erling; Tempelaar, Roel; Alcocer, Marcelo J. P. Nature Chemistry, Vol. 10, Issue 7 https://doi.org/10.1038/s41557-018-0060-5	journal	May 2018
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Origin of long-lived oscillations in 2D-spectra of a quantum vibronic model: Electronic versus vibrational coherence Plenio, M. B.; Almeida, J.; Huelga, S. F. The Journal of Chemical Physics, Vol. 139, Issue 23 https://doi.org/10.1063/1.4846275	journal	December 2013
Vibronic phenomena and exciton–vibrational interference in two-dimensional spectra of molecular aggregates Butkus, Vytautas; Valkunas, Leonas; Abramavicius, Darius The Journal of Chemical Physics, Vol. 140, Issue 3 https://doi.org/10.1063/1.4861466	journal	January 2014
Resolving molecular vibronic structure using high-sensitivity two-dimensional electronic spectroscopy Bizimana, Laurie A.; Brazard, Johanna; Carbery, William P. The Journal of Chemical Physics, Vol. 143, Issue 16 https://doi.org/10.1063/1.4934717	journal	October 2015
Effects of Herzberg–Teller vibronic coupling on coherent excitation energy transfer Zhang, Hou-Dao; Qiao, Qin; Xu, Rui-Xue The Journal of Chemical Physics, Vol. 145, Issue 20 https://doi.org/10.1063/1.4968031	journal	November 2016
Signatures of vibronic coupling in two-dimensional electronic-vibrational and vibrational-electronic spectroscopies Gaynor, James D.; Khalil, Munira The Journal of Chemical Physics, Vol. 147, Issue 9 https://doi.org/10.1063/1.4991745	journal	September 2017
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
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