Quantum coherent energy transport in the Fenna–Matthews–Olson complex at low temperature

Duan, H.-G., Jha, A., Chen, L., Tiwari, V., Cogdell, R. J. , Ashraf, K., Prokhorenko, V. I., Thorwart, M. and Miller, R. J. D. (2022) Quantum coherent energy transport in the Fenna–Matthews–Olson complex at low temperature. Proceedings of the National Academy of Sciences of the United States of America, 119(49), e2212630119. (doi: 10.1073/pnas.2212630119) (PMID:36442134) (PMCID:PMC9894199)

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Abstract

In the primary step of natural light harvesting, the solar photon energy is captured in a photoexcited electron–hole pair, or an exciton, in chlorophyll. Its conversion to chemical potential occurs in the special pair reaction center, which is reached by downhill ultrafast excited-state energy transport through a network of chromophores. Being inherently quantum, transport could in principle occur via a matter wave, with vast implications for efficiency. How long a matter wave remains coherent is determined by the intensity by which the exciton is disturbed by the noisy biological environment. The stronger this is, the stronger the electronic coupling between chromophores must be to overcome the fluctuations and phase shifts. The current consensus is that under physiological conditions, quantum coherence vanishes on the 10-fs time scale, rendering it irrelevant for the observed picosecond transfer. Yet, at low-enough temperature, quantum coherence should in principle be present. Here, we reveal the onset of longer-lived electronic coherence at extremely low temperatures of ∼20 K. Using two-dimensional electronic spectroscopy, we determine the exciton coherence times in the Fenna–Matthew–Olson complex over an extensive temperature range. At 20 K, coherence persists out to 200 fs (close to the antenna) and marginally up to 500 fs at the reaction center. It decays markedly faster with modest increases in temperature to become irrelevant above 150 K. At low temperature, the fragile electronic coherence can be separated from the robust vibrational coherence, using a rigorous theoretical analysis. We believe that by this generic principle, light harvesting becomes robust against otherwise fragile quantum effects.

Item Type:Articles
Additional Information:This work was supported by the Max Planck Society and the Excellence Cluster “CUI: Advanced Imaging of Matter” of the Deutsche Forschungsgemeinschaft (DFG)–EXC 2056–project ID 390715994. K.A. and R.J.C. acknowledge funding by “The Photosynthetic Antenna Research Center” under the US DoE Energy Frontier Research Center grant number DE-SC 0001035. Lipeng Chen was supported by the Key Research Project of Zhejiang Lab (No. 2021PE0AC02).
Keywords:Energy transfer, two-dimensional spectroscopy, excitonic coupling, coherent transport.
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Cogdell, Professor Richard and Ashraf, Mr Khuram
Authors: Duan, H.-G., Jha, A., Chen, L., Tiwari, V., Cogdell, R. J., Ashraf, K., Prokhorenko, V. I., Thorwart, M., and Miller, R. J. D.
College/School:College of Medical Veterinary and Life Sciences > School of Molecular Biosciences
Journal Name:Proceedings of the National Academy of Sciences of the United States of America
Publisher:National Academy of Sciences
ISSN:0027-8424
ISSN (Online):1091-6490
Published Online:28 November 2022
Copyright Holders:Copyright © 2022 The Authors
First Published:First published in Proceedings of the National Academy of Sciences of the United States of America 119(49): e2212630119
Publisher Policy:Reproduced under a Creative Commons License

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