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Vibronic coherence in oxygenic photosynthesis

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Abstract

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.

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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.

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Acknowledgements

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).

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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.

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The authors declare no competing financial interests.

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Fuller, F., Pan, J., Gelzinis, A. et al. Vibronic coherence in oxygenic photosynthesis. Nature Chem 6, 706–711 (2014). https://doi.org/10.1038/nchem.2005

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