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Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection

Nature Chemistry volume 9, pages 772–778 (2017)Cite this article

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Abstract

In oxygenic photosynthesis, light harvesting is regulated to safely dissipate excess energy and prevent the formation of harmful photoproducts. Regulation is known to be necessary for fitness, but the molecular mechanisms are not understood. One challenge has been that ensemble experiments average over active and dissipative behaviours, preventing identification of distinct states. Here, we use single-molecule spectroscopy to uncover the photoprotective states and dynamics of the light-harvesting complex stress-related 1 (LHCSR1) protein, which is responsible for dissipation in green algae and moss. We discover the existence of two dissipative states. We find that one of these states is activated by pH and the other by carotenoid composition, and that distinct protein dynamics regulate these states. Together, these two states enable the organism to respond to two types of intermittency in solar intensity—step changes (clouds and shadows) and ramp changes (sunrise), respectively. Our findings reveal key control mechanisms underlying photoprotective dissipation, with implications for increasing biomass yields and developing robust solar energy devices.

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Figure 1: Time traces of fluorescence intensity and lifetime of LHCSR1 and LHCB1.
Figure 2: Fluorescence intensity–lifetime probability distributions of single LHCSR1 and LHCB1 reveal protein dynamics.
Figure 3: Cartoon illustration of the free-energy landscape of LHCSR1.
Figure 4: Potential scheme of light-harvesting activity regulated through LHCSR1.

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Acknowledgements

This work was supported as part of the Center for Excitonics, an Energy Frontier Research Center funded by the US Department of Energy, Office of Science, Office of Basic Energy Sciences under award no. DE-SC0001088 (MIT) and a CIFAR Azrieli Global Scholar Award to G.S.S.-C., and the EEC projects ACCLIPHOT (PITN-GA-2012-316427) and SE2B (675006-SE2B) to R.B.

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Authors and Affiliations

  1. Department of Chemistry, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, 02139, Massachusetts, USA

    Toru Kondo, Wei Jia Chen & Gabriela S. Schlau-Cohen

  2. Department of Biotechnology, University of Verona, Ca' Vignal 1, Strada Le Grazie 15, Verona, 37134, Italy

    Alberta Pinnola, Luca Dall'Osto & Roberto Bassi

  3. Istituto per la Protezione delle Piante (IPP), Consiglio Nazionale delle Ricerche (CNR), Strada delle Cacce 73, Turin, 10135, Italy

    Roberto Bassi

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Contributions

T.K., R.B. and G.S.S.-C. conceived and designed the experiments. T.K. and W.J.C. performed the experiments. T.K. and G.S.S.-C. analysed the data. A.P., L.D. and R.B. contributed materials and analysis tools. T.K. and G.S.S.-C. co-wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Gabriela S. Schlau-Cohen.

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Kondo, T., Pinnola, A., Chen, W. et al. Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection. Nature Chem 9, 772–778 (2017). https://doi.org/10.1038/nchem.2818

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