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Direct observation of subpicosecond vibrational dynamics in photoexcited myoglobin

Nature Chemistry volume 8, pages 1137–1143 (2016)Cite this article

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Abstract

Determining the initial pathway for ultrafast energy redistribution within biomolecules is a challenge, and haem proteins, for which energy can be deposited locally in the haem moiety using short light pulses, are suitable model systems to address this issue. However, data acquired using existing experimental techniques that fail to combine sufficient structural sensitivity with adequate time resolution have resulted in alternative hypotheses concerning the interplay between energy flow among highly excited vibrational levels and potential concomitant electronic processes. By developing a femtosecond-stimulated Raman set-up, endowed with the necessary tunability to take advantage of different resonance conditions, here we visualize the temporal evolution of energy redistribution over different vibrational modes in myoglobin. We establish that the vibrational energy initially stored in the highly excited Franck–Condon manifold is transferred with different timescales into low- and high-frequency modes, prior to slow dissipation through the protein. These findings demonstrate that a newly proposed mechanism involving the population dynamics of specific vibrational modes settles the controversy on the existence of transient electronic intermediates.

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Figure 1: Haem photolysis/photoexcitation.
Figure 2: TA experiment in deoxy-Mb.
Figure 3: FSRRS snapshots of vibrational-energy flow in Mb.
Figure 4: Modelling subpicosecond vibrational dynamics in Mb.
Figure 5: Proposed energy-transfer mechanism in Mb.

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Acknowledgements

T.S. thanks A. Arcovito for early discussions on the potential impact of an FSRS experiment in Mb, and acknowledges an inspiring visit to the Mathies lab. M. Aschi, G. Batignani, P. Champion, M. Garavelli, P. Kukura, Y. Mizutani, S. Kruglik and S. Mukamel provided invaluable input to this work. The authors thank B. Vallone and the Dipartimento di Scienze Biochimiche and Istituto Pasteur-Fondazione Cenci Bolognetti of Università di Roma La Sapienza for support with the sample preparation. T.S. is especially grateful to M. Brunori for continued support and critical insights. This research has received funding from the European Research Council under the European Union Seventh Framework Program (FP7/2007–2013) and no. 207916 (FEMTOSCOPY).

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Authors and Affiliations

  1. Dipartimento di Fisica, Università di Roma, La Sapienza, Roma, I-00185, Italy

    C. Ferrante, E. Pontecorvo & T. Scopigno

  2. Dipartimento di Fisica, Istituto di Fotonica e Nanotecnologie (IFN-CNR), Politecnico di Milano, Piazza L. da Vinci 32, Milano, 20133, Italy

    G. Cerullo

  3. LOB, Ecole Polytechnique, CNRS, INSERM, Université Paris-Saclay, Palaiseau Cedex, 91128, France

    M. H. Vos

  4. Center for Life Nano Science@Sapienza, Istituto Italiano di Tecnologia, Rome, Viale Regina Elena 291, 00161, Italy

    T. Scopigno

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Contributions

T.S. directed the research. E.P. led the experimental activity with the assistance of C.F. and support from G.C. and T.S. C.F. performed data analysis and numerical modelling with the assistance of E.P. T.S. wrote the manuscript with C.F. and M.H.V. All the authors discussed the results and implications and commented on the manuscript.

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Correspondence to T. Scopigno.

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Ferrante, C., Pontecorvo, E., Cerullo, G. et al. Direct observation of subpicosecond vibrational dynamics in photoexcited myoglobin. Nature Chem 8, 1137–1143 (2016). https://doi.org/10.1038/nchem.2569

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