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Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems

Abstract

Photosynthetic complexes are exquisitely tuned to capture solar light efficiently, and then transmit the excitation energy to reaction centres, where long term energy storage is initiated. The energy transfer mechanism is often described by semiclassical models that invoke ‘hopping’ of excited-state populations along discrete energy levels1,2. Two-dimensional Fourier transform electronic spectroscopy3,4,5 has mapped6 these energy levels and their coupling in the Fenna–Matthews–Olson (FMO) bacteriochlorophyll complex, which is found in green sulphur bacteria and acts as an energy ‘wire’ connecting a large peripheral light-harvesting antenna, the chlorosome, to the reaction centre7,8,9. The spectroscopic data clearly document the dependence of the dominant energy transport pathways on the spatial properties of the excited-state wavefunctions of the whole bacteriochlorophyll complex6,10. But the intricate dynamics of quantum coherence, which has no classical analogue, was largely neglected in the analyses—even though electronic energy transfer involving oscillatory populations of donors and acceptors was first discussed more than 70 years ago11, and electronic quantum beats arising from quantum coherence in photosynthetic complexes have been predicted12,13 and indirectly observed14. Here we extend previous two-dimensional electronic spectroscopy investigations of the FMO bacteriochlorophyll complex, and obtain direct evidence for remarkably long-lived electronic quantum coherence playing an important part in energy transfer processes within this system. The quantum coherence manifests itself in characteristic, directly observable quantum beating signals among the excitons within the Chlorobium tepidum FMO complex at 77 K. This wavelike characteristic of the energy transfer within the photosynthetic complex can explain its extreme efficiency, in that it allows the complexes to sample vast areas of phase space to find the most efficient path.

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Figure 1: Two-dimensional electronic spectra of FMO.
Figure 2: Electronic coherence beating.
Figure 3: Characteristic anticorrelation between peak amplitude and width.
Figure 4: Quantum beating in cross peaks.

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Acknowledgements

We thank D. Zigmantas for discussions and J. Wen for purification of the sample. This work was supported by the DOE (at LBNL, UC Berkeley and Washington Univ.). G.S.E. thanks the Miller Institute for Basic Research in Science for support. T.-K.A. was supported by the Korea Research Foundation Grant funded by the Korean government (MOEHRD).

Author Contributions G.S.E, T.R.C., T.-K.A. and E.L.R. prepared the cryogenic sample and collected the data; G.S.E., E.L.R, T.M. and Y.-C.C. performed the data analysis. R.E.B. grew, isolated and purified the FMO sample. G.S.E. wrote the paper, and all authors discussed the results and commented on the manuscript. G.R.F. provided guidance throughout the experiment and analysis and helped to write the manuscript.

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Correspondence to Graham R. Fleming.

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Supplementary information

Supplementary Figures

This file contains Supplementary Figures 1-2 with Legends and Supplementary Movie Legend. (PDF 850 kb)

Supplementary Movie 1

This file contains Supplementary Movie 1. The Supplementary Movie shows spectral evolution of the FMO 2D Electronic spectra with ultrafast time resolution. Data from 33 time points is linearly interpolated to create this movie. (MOV 12750 kb)

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Engel, G., Calhoun, T., Read, E. et al. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446, 782–786 (2007). https://doi.org/10.1038/nature05678

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