Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems (2024)

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Abstract Access options Additional access options: Similar content being viewed by others Quantum coherences reveal excited-state dynamics in biophysical systems Vibronic mixing enables ultrafast energy flow in light-harvesting complex II Excitation energy transfer and vibronic coherence in intact phycobilisomes References Acknowledgements Author information Authors and Affiliations Corresponding author Ethics declarations Competing interests Supplementary information Supplementary Figures Supplementary Movie 1 Rights and permissions About this article Cite this article This article is cited by Quantum-walk search in motion Need of Quantum Biology to Investigate Beneficial Effects at Low Doses (< 100 mSv) and Maximize Peaceful Applications of Nuclear Energy Open system approach to neutrino oscillations in a quantum walk framework Experimental demonstration of attosecond pump–probe spectroscopy with an X-ray free-electron laser Essential role of momentum-forbidden dark excitons in the energy transfer responses of monolayer transition-metal dichalcogenides Comments
  • Letter
  • Published:
  • Gregory S. Engel1,2,
  • Tessa R. Calhoun1,2,
  • Elizabeth L. Read1,2,
  • Tae-Kyu Ahn1,2,
  • Tomáš Mančal1,2nAff5,
  • Yuan-Chung Cheng1,2,
  • Robert E. Blankenship3,4 &
  • …
  • Graham R. Fleming1,2

Nature volume446,pages 782–786 (2007)Cite this article

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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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Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems (1)
Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems (2)
Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems (3)
Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems (4)

Similar content being viewed by others

Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems (5)

Quantum coherences reveal excited-state dynamics in biophysical systems

Article 24 June 2019

Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems (7)

Excitation energy transfer and vibronic coherence in intact phycobilisomes

Article 19 September 2022

References

  1. Blankenship, R. E. Molecular Mechanisms of Photosynthesis (Blackwell Science, Oxford/Malden, 2002)

    Book Google Scholar

  2. van Amerongen, H., Valkunas, L. & van Grondelle, R. Photosynthetic Excitons (World Scientific, Singapore/River Edge, 2000)

    Book Google Scholar

  3. Brixner, T., Mančal, T., Stiopkin, I. V. & Fleming, G. R. Phase-stabilized two-dimensional electronic spectroscopy. J. Chem. Phys. 121, 4221–4236 (2004)

    Article ADS CAS Google Scholar

  4. Jonas, D. M. Two-dimensional femtosecond spectroscopy. Annu. Rev. Phys. Chem. 54, 425–463 (2003)

    Article ADS CAS Google Scholar

  5. Cowan, M. L., Ogilvie, J. P. & Miller, R. J. D. Two-dimensional spectroscopy using diffractive optics based phased-locked photon echoes. Chem. Phys. Lett. 386, 184–189 (2004)

    Article ADS CAS Google Scholar

  6. Brixner, T. et al. Two-dimensional spectroscopy of electronic couplings in photosynthesis. Nature 434, 625–628 (2005)

    Article ADS CAS Google Scholar

  7. Fenna, R. E. & Matthews, B. W. Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola. Nature 258, 573–577 (1975)

    Article ADS CAS Google Scholar

  8. Li, Y. F., Zhou, W. L., Blankenship, R. E. & Allen, J. P. Crystal structure of the bacteriochlorophyll a protein from Chlorobium tepidum. J. Mol. Biol. 271, 456–471 (1997)

    Article CAS Google Scholar

  9. Camara-Artigas, A., Blankenship, R. E. & Allen, J. P. The structure of the FMO protein from Chlorobium tepidum at 2.2 angstrom resolution. Photosynth. Res. 75, 49–55 (2003)

    Article CAS Google Scholar

  10. Cho, M. H. et al. Exciton analysis in 2D electronic spectroscopy. J. Phys. Chem. B 109, 10542–10556 (2005)

    Article CAS Google Scholar

  11. Perrin, F. Thoérie quantique des transferts d'activation entre molécules de même espèce. Cas des solutions fluorescentes. Ann. Phys. (Paris) 17, 283–314 (1932)

    ADS CAS MATH Google Scholar

  12. Knox, R. S. Electronic excitation transfer in the photosynthetic unit: Reflections on work of William Arnold. Photosynth. Res. 48, 35–39 (1996)

    Article CAS Google Scholar

  13. Leegwater, J. A. Coherent versus incoherent energy transfer and trapping in photosynthetic antenna complexes. J. Phys. Chem. 100, 14403–14409 (1996)

    Article CAS Google Scholar

  14. Savikhin, S., Buck, D. R. & Struve, W. S. Oscillating anisotropies in a bacteriochlorophyll protein: Evidence for quantum beating between exciton levels. Chem. Phys. 223, 303–312 (1997)

    Article CAS Google Scholar

  15. Brixner, T., Stiopkin, I. V. & Fleming, G. R. Tunable two-dimensional femtosecond spectroscopy. Opt. Lett. 29, 884–886 (2004)

    Article ADS CAS Google Scholar

  16. Cho, M. H. & Fleming, G. R. The integrated photon echo and solvation dynamics. II. Peak shifts and two-dimensional photon echo of a coupled chromophore system. J. Chem. Phys. 123, 114506 (2005)

    Article ADS Google Scholar

  17. Pisliakov, A. V., Mančal, T. & Fleming, G. R. Two-dimensional optical three-pulse photon echo spectroscopy. II. Signatures of coherent electronic motion and exciton population transfer in dimer two-dimensional spectra. J. Chem. Phys. 124, 234505 (2006)

    Article ADS Google Scholar

  18. Abramavicius, D., Valkunas, L. & van Grondelle, R. Exciton dynamics in ring-like photosynthetic light-harvesting complexes: A hopping model. Phys. Chem. Chem. Phys. 6, 3097–3105 (2004)

    Article CAS Google Scholar

  19. Renger, T., May, V. & Kuhn, O. Ultrafast excitation energy transfer dynamics in photosynthetic pigment-protein complexes. Phys. Rep. Rev. Phys. Lett. 343, 138–254 (2001)

    Google Scholar

  20. Jang, S. J., Newton, M. D. & Silbey, R. J. Multichromophoric Forster resonance energy transfer. Phys. Rev. Lett. 92, 9312–9323 (2004)

    Google Scholar

  21. Novoderezhkin, V., Wendling, M. & van Grondelle, R. Intra- and interband transfers in the b800-b850 antenna of Rhodospirillum molischianum: Redfield theory modeling of polarized pump-probe kinetics. J. Phys. Chem. B 107, 11534–11548 (2003)

    Article CAS Google Scholar

  22. Vulto, S. I. E. et al. Excited state dynamics in FMO antenna complexes from photosynthetic green sulfur bacteria: A kinetic model. J. Phys. Chem. B 103, 8153–8161 (1999)

    Article CAS Google Scholar

  23. Potts, D. & Kunis, S. Stability results for scattered data interpolation by trigonometric polynomials. 〈http://arxiv.org/pdf/math.NA/0702019〉 (2007)

  24. Dreyer, J., Moran, A. M. & Mukamel, S. Tensor components in three pulse vibrational echoes of a rigid dipeptide. Bull. Korean Chem. Soc. 24, 1091–1096 (2003)

    Article CAS Google Scholar

  25. Hochstrasser, R. M. Two-dimensional IR-spectroscopy: polarization anisotropy effects. Chem. Phys. 266, 273–284 (2001)

    Article CAS Google Scholar

  26. Kempe, J. Quantum random walks: An introductory overview. Contemp. Phys. 44, 307–327 (2003)

    Article ADS Google Scholar

  27. Grover, L. K. Quantum mechanics helps in searching for a needle in a haystack. Phys. Rev. Lett. 79, 325–328 (1997)

    Article ADS CAS Google Scholar

  28. Joo, T., Jia, Y. W. & Fleming, G. R. Ti-sapphire regenerative amplifier for ultrashort high-power multikilohertz pulses without an external stretcher. Opt. Lett. 20, 389–391 (1995)

    Article ADS CAS Google Scholar

  29. Lepetit, L., Cheriaux, G. & Joffre, M. Linear techniques of phase measurement by femtosecond spectral interferometry for applications in spectroscopy. J. Opt. Soc. Am. B 12, 2467–2474 (1995)

    Article ADS CAS Google Scholar

  30. Frigo, M. & Johnson, S. G. The design and implementation of fftw3. Proc. IEEE 93, 216–231 (2005)

    Article Google Scholar

Download references

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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Author notes

  1. Tomáš Mančal

    Present address: Present address: Institute of Physics of Charles University, 12116 Prague 2, Czech Republic.,

Authors and Affiliations

  1. Department of Chemistry & QB3 Institute, University of California, Berkeley,

    Gregory S. Engel,Tessa R. Calhoun,Elizabeth L. Read,Tae-Kyu Ahn,Tomáš Mančal,Yuan-Chung Cheng&Graham R. Fleming

  2. Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA,

    Gregory S. Engel,Tessa R. Calhoun,Elizabeth L. Read,Tae-Kyu Ahn,Tomáš Mančal,Yuan-Chung Cheng&Graham R. Fleming

  3. Department of Biology,,

    Robert E. Blankenship

  4. Department of Chemistry, Washington University, St Louis, Missouri 63130, USA,

    Robert E. Blankenship

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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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Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems (2024)
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