Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Vibronic coherence in oxygenic photosynthesis



Photosynthesis powers life on our planet. The basic photosynthetic architecture consists of antenna complexes that harvest solar energy and reaction centres that convert the energy into stable separated charge. In oxygenic photosynthesis, the initial charge separation occurs in the photosystem II reaction centre, the only known natural enzyme that uses solar energy to split water. Both energy transfer and charge separation in photosynthesis are rapid events with high quantum efficiencies. In recent nonlinear spectroscopic experiments, long-lived coherences have been observed in photosynthetic antenna complexes, and theoretical work suggests that they reflect underlying electronic–vibrational resonances, which may play a functional role in enhancing energy transfer. Here, we report the observation of coherent dynamics persisting on a picosecond timescale at 77 K in the photosystem II reaction centre using two-dimensional electronic spectroscopy. Supporting simulations suggest that the coherences are of a mixed electronic–vibrational (vibronic) nature and may enhance the rate of charge separation in oxygenic photosynthesis.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: 2DES of the photosystem II reaction centre at 77 K, revealing coherent dynamics at a number of frequencies.
Figure 2: Comparison of the frequencies obtained from 2DES measurements with exciton difference frequencies and vibrational modes, providing insight into the physical origin of the observed coherent dynamics.
Figure 3: Coherence amplitude maps (filled contours) reveal the distribution of the observed coherent dynamics throughout the 2D spectra.
Figure 4: Simulated coherence amplitude maps (filled contours) for comparison with the experimental coherence maps shown in Fig. 3.
Figure 5: Simulations to examine the effect of the frequency and coherent/incoherent nature of different vibrational modes on charge separation.


  1. 1

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

    CAS  Article  Google Scholar 

  2. 2

    Turner, D. B. et al. Quantitative investigations of quantum coherence for a light-harvesting protein at conditions simulating photosynthesis. Phys. Chem. Chem. Phys. 14, 4857–4874 (2012).

    CAS  Article  Google Scholar 

  3. 3

    Scholes, G. D., Fleming, G. R., Olaya-Castro, A. & van Grondelle, R. Lessons from nature about solar light harvesting. Nature Chem. 3, 763–774 (2011).

    CAS  Article  Google Scholar 

  4. 4

    Lewis, K. L. M. & Ogilvie, J. P. Probing photosynthetic energy and charge transfer with two-dimensional electronic spectroscopy. J. Phys. Chem. Lett. 3, 503–510 (2012).

    CAS  Article  Google Scholar 

  5. 5

    Engel, G. S. et al. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446, 782–786 (2007).

    CAS  Article  Google Scholar 

  6. 6

    Panitchayangkoon, G. et al. Long-lived quantum coherence in photosynthetic complexes at physiological temperature. Proc. Natl Acad. Sci. USA 107, 12766–12770 (2010).

    CAS  Article  Google Scholar 

  7. 7

    Collini, E. & Scholes, G. D. Coherent intrachain energy migration in a conjugated polymer at room temperature. Science 323, 369–373 (2009).

    CAS  Article  Google Scholar 

  8. 8

    Milota, F. et al. Vibronic and vibrational coherences in two-dimensional electronic spectra of supramolecular J-aggregates. J. Phys. Chem. A 117, 6007–6014 (2013).

    CAS  Article  Google Scholar 

  9. 9

    Valkunas, L., Abramavicius, D. & Mancal, T. Molecular Excitation Dynamics and Relaxation (Wiley-VCH, 2013).

    Book  Google Scholar 

  10. 10

    Chenu, A., Christensson, N., Kauffmann, H. F. & Mancal, T. Enhancement of vibronic and ground-state vibrational coherences in 2D spectra of photosynthetic complexes. Sci. Rep. 3, 2029 (2013).

    Article  Google Scholar 

  11. 11

    Christensson, N., Kauffmann, H. F., Pullerits, T. & Mancal, T. Origin of long-lived coherences in light-harvesting complexes. J. Phys. Chem. B 116, 7449–7454 (2012).

    CAS  Article  Google Scholar 

  12. 12

    Butkus, V., Valkunas, L. & Abramavicius, D. Vibronic phenomena and exciton–vibrational interference in two-dimensional spectra of molecular aggregates. J. Chem. Phys. 140, 034306 (2014).

    Article  Google Scholar 

  13. 13

    Butkus, V., Zigmantas, D., Abramavicius, D. & Valkunas, L. Distinctive character of electronic and vibrational coherences in disordered molecular aggregates. Chem. Phys. Lett. 587, 93–98 (2013).

    CAS  Article  Google Scholar 

  14. 14

    Butkus, V., Zigmantas, D., Valkunas, L. & Abramavicius, D. Vibrational vs. electronic coherences in 2D spectrum of molecular systems. Chem. Phys. Lett. 545, 40–43 (2012).

    CAS  Article  Google Scholar 

  15. 15

    Tiwari, V., Peters, W. K. & Jonas, D. M. Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework. Proc. Natl Acad. Sci. USA 110, 1203–1208 (2013).

    CAS  Article  Google Scholar 

  16. 16

    Halpin, A. et al. Two-dimensional spectroscopy of a molecular dimer unveils the effects of vibronic coupling on exciton coherences. Nature Chem. 6, 196–201 (2014).

    CAS  Article  Google Scholar 

  17. 17

    Womick, J. M. & Moran, A. M. Vibronic enhancement of exciton sizes and energy transport in photosynthetic complexes. J. Phys. Chem. B 115, 1347–1356 (2011).

    CAS  Article  Google Scholar 

  18. 18

    Kolli, A., O'Reilly, E. J., Scholes, G. D. & Olaya-Castro, A. The fundamental role of quantized vibrations in coherent light harvesting by cryptophyte algae. J. Chem. Phys. 137, 174109 (2012).

    Article  Google Scholar 

  19. 19

    Huelga, S. F. & Plenio, M. B. Vibrations, quanta and biology. Contemp. Phys. 54, 181–207 (2013).

    CAS  Article  Google Scholar 

  20. 20

    Renaud, N. et al. Quantum interferences and electron transfer in photosystem I. J. Phys. Chem. A 117, 5899–5908 (2013).

    CAS  Article  Google Scholar 

  21. 21

    Pan, J. et al. The protein environment of the bacteriopheophytin anion modulates charge separation and charge recombination in bacterial reaction centers. J. Phys. Chem. B 117, 7179–7189 (2013).

    CAS  Article  Google Scholar 

  22. 22

    Lee, H., Cheng, Y. C. & Fleming, G. R. Coherence dynamics in photosynthesis: protein protection of excitonic coherence. Science 316, 1462–1465 (2007).

    CAS  Article  Google Scholar 

  23. 23

    Westenhoff, S., Palecek, D., Edlund, P., Smith, P. & Zigmantas, D. Coherent picosecond exciton dynamics in a photosynthetic reaction center. J. Am. Chem. Soc. 134, 16484–16487 (2012).

    CAS  Article  Google Scholar 

  24. 24

    Ryu, I. S., Dong, H. & Fleming, G. R. Role of electronic–vibrational mixing in enhancing vibrational coherences in the ground electronic states of photosynthetic bacterial reaction center. J. Phys. Chem. B 118, 1381–1388 (2014).

    CAS  Article  Google Scholar 

  25. 25

    Vos, M. H. et al. Direct observation of vibrational coherence in bacterial reaction centers using femtosecond absorption spectroscopy. Proc. Natl Acad. Sci. USA 88, 8885–8889 (1991).

    CAS  Article  Google Scholar 

  26. 26

    Vos, M. H., Rappaport, F., Lambry, J. C., Breton, J. & Martin, J. L. Visualization of coherent nuclear motion in a membrane protein by femtosecond spectroscopy. Nature 363, 320–325 (1993).

    CAS  Article  Google Scholar 

  27. 27

    Lewis, K. L. M. et al. Simulations of the two-dimensional electronic spectroscopy of the photosystem II reaction center. J. Phys. Chem. A 117, 34–41 (2013).

    CAS  Article  Google Scholar 

  28. 28

    Gelzinis, A. et al. Tight-binding model of the photosystem II reaction center: application to two-dimensional electronic spectroscopy. New J. Phys. 15, 075013 (2013).

    Article  Google Scholar 

  29. 29

    Myers, J. A. et al. Two-dimensional electronic spectroscopy of the D1-D2-cyt b559 photosystem II reaction center complex. J. Phys. Chem. Lett. 1, 2774–2780 (2010).

    CAS  Article  Google Scholar 

  30. 30

    Novoderezhkin, V. I., Dekker, J. P. & van Grondelle, R . Mixing of exciton and charge-transfer states in photosystem II reaction centers: modeling of Stark spectra with modified Redfield theory. Biophys. J. 93, 1293–1311 (2007).

    CAS  Article  Google Scholar 

  31. 31

    Peterman, E. J. G., van Amerongen, H., van Grondelle, R. & Dekker, J. P. The nature of the excited state of the reaction center of photosystem II of green plants: a high-resolution fluorescence spectroscopy study. Proc. Natl Acad. Sci. USA 95, 6128–6133 (1998).

    CAS  Article  Google Scholar 

  32. 32

    Picorel, R., Chumanov, G., Torrado, E., Cotton, T. M. & Seibert, M. Surface-enhanced resonance Raman scattering spectroscopy of plant photosystem II reaction centers excited on the red-edge of the Q(y) band. J. Phys. Chem. B 102, 2609–2613 (1998).

    CAS  Article  Google Scholar 

  33. 33

    Ando, K. & Sumi, H. Nonequilibrium oscillatory electron transfer in bacterial photosynthesis. J. Phys. Chem. B 102, 10991–11000 (1998).

    CAS  Article  Google Scholar 

  34. 34

    Novoderezhkin, V. I., Yakovlev, A. G., van Grondelle, R. & Shuvalov, V. A. Coherent nuclear and electronic dynamics in primary charge separation in photosynthetic reaction centers: a Redfield theory approach. J. Phys. Chem. B 108, 7445–7457 (2004).

    CAS  Article  Google Scholar 

  35. 35

    Romero, E., van Stokkum, I. H. M., Novoderezhkin, V. I., Dekker, J. P. & van Grondelle, R. Two different charge separation pathways in photosystem II. Biochemistry 49, 4300–4307 (2010).

    CAS  Article  Google Scholar 

  36. 36

    Shelaev, I. V. et al. Primary light-energy conversion in tetrameric chlorophyll structure of photosystem II and bacterial reaction centers: II. Femto-and picosecond charge separation in PSII D1/D2/Cyt b559 complex. Photosynth. Res. 98, 95–103 (2008).

    CAS  Article  Google Scholar 

  37. 37

    Tanimura, Y. Reduced hierarchy equations of motion approach with Drude plus Brownian spectral distribution: probing electron transfer processes by means of two-dimensional correlation spectroscopy. J. Chem. Phys. 137, 22A550 (2012).

    Article  Google Scholar 

  38. 38

    Abramavicius, D., Gulbinas, V. & Valkunas, L. Acceleration of charge separation by oscillations of the environment polarization. Chem. Phys. Lett. 368, 480–485 (2003).

    CAS  Article  Google Scholar 

  39. 39

    Fuller, F. D., Wilcox, D. E. & Ogilvie, J. P. Pulse shaping based two-dimensional electronic spectroscopy in a background free geometry. Opt. Express 22, 1018–1027 (2014).

    Article  Google Scholar 

Download references


F.D.F., J.P. and J.P.O. acknowledge support from the Office of Basic Energy Sciences, the US Department of Energy (grant no. DE-FG02-07ER15904). S.S.S. acknowledges support from the National Science Foundation (grant no. PHY-0748470). D.E.W. acknowledges support from the Center for Solar and Thermal Energy Conversion (CSTEC), an Energy Frontier Research Center funded by the US Department of Energy (DOE), Office of Science, Basic Energy Sciences (award no. DE-SC0000957). A.G., V.B., L.V. and D.A. acknowledge support from the Research Council of Lithuania (LMT grant no. MIP-069/2012).

Author information




F.D.F. and J.P.O. conceived and designed the experiments. F.D.F., J.P. and S.S.S. performed the experiments. F.D.F. analysed the data. D.E.W. contributed to data fitting and debugging of the optical set-up. A.G., V.B., L.V. and D.A. designed and performed simulations and considered their correspondence to the experimental data. F.D.F. and J.P.O. wrote the manuscript, with input from all the authors.

Corresponding author

Correspondence to Jennifer P. Ogilvie.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information (PDF 5401 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fuller, F., Pan, J., Gelzinis, A. et al. Vibronic coherence in oxygenic photosynthesis. Nature Chem 6, 706–711 (2014).

Download citation

Further reading


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing