Programmed coherent coupling in a synthetic DNA-based excitonic circuit

Abstract

Natural light-harvesting systems spatially organize densely packed chromophore aggregates using rigid protein scaffolds to achieve highly efficient, directed energy transfer. Here, we report a synthetic strategy using rigid DNA scaffolds to similarly program the spatial organization of densely packed, discrete clusters of cyanine dye aggregates with tunable absorption spectra and strongly coupled exciton dynamics present in natural light-harvesting systems. We first characterize the range of dye-aggregate sizes that can be templated spatially by A-tracts of B-form DNA while retaining coherent energy transfer. We then use structure-based modelling and quantum dynamics to guide the rational design of higher-order synthetic circuits consisting of multiple discrete dye aggregates within a DX-tile. These programmed circuits exhibit excitonic transport properties with prominent circular dichroism, superradiance, and fast delocalized exciton transfer, consistent with our quantum dynamics predictions. This bottom-up strategy offers a versatile approach to the rational design of strongly coupled excitonic circuits using spatially organized dye aggregates for use in coherent nanoscale energy transport, artificial light-harvesting, and nanophotonics.

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Figure 1: Schematic overview of the overall design and validation framework of DNA-based excitonic circuits with enhanced energy transport.
Figure 2: Integrated experimental–computational characterization of elementary J-aggregate building blocks.
Figure 3: Structure-based computational design and experimental characterization of a synthetic multi-J-bit excitonic circuit.
Figure 4: Programming two- and three-step energy transfer within the multi-J-bit excitonic circuit.

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Acknowledgements

We are grateful for fruitful conversations with M. Adendorff, S. Ratanalert, T. Fujita, S. Valleau and J. Suh. Funding from the ARO MURI W911NF1210420 to M.B., N.W.W. and H.Y. is gratefully acknowledged. This work received support to M.B., G.S.S.C. and A.A.-G. from the MIT Center for Excitonics, an Energy Frontier Research Center funded by the US Department of Energy under award DE-SC0001088. M.B. additionally acknowledges funding from ONR DURIP N00014-16-1-2506 and ONR N00014-16-1-2181. A portion of the simulations was performed on Harvard University’s Odyssey cluster, supported by the Research Computing Group of the FAS Division of Science. Some of the hardware used was provided by Harvard University’s CUDA Center of Excellence (CCOE) Program, sponsored by NVIDIA. N.S. acknowledges funding from the Smith Family Graduate Science and Engineering Fellowship. The Biophysical Instrumentation Facility for the Study of Complex Macromolecular Systems (NSF-0070319) is gratefully acknowledged. E.B. acknowledges funding from the Natural Sciences and Engineering Research Council of Canada (NSERC).

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E.B. designed and performed molecular modelling and exciton transport simulations, designed and performed CD experiments, designed UV–vis and fluorescence spectroscopy experiments, and analysed the data. N.S. designed and performed the simulations for excitonic properties and exciton transport, and analysed the data. R.V. designed and performed UV–vis and CD experiments, ITC experiments, designed the fluorescence spectroscopy experiments, prepared the samples, and analysed the data. J.L.B. designed and performed quantum yield measurements to measure the coherence length and steady-state fluorescence spectroscopy to measure energy transfer efficiency. T.K. designed and performed experiments to measure energy transfer efficiencies using time-resolved fluorescence spectroscopy. G.S.S.C. designed and supervised the experiments to measure the coherence length and energy transfer efficiencies using steady-state and time-resolved spectroscopy. A.A., S.M. and S.L. designed and performed the fluorescence and pump–probe spectroscopy experiments, and analysed the data. N.W. designed and supervised the fluorescence and pump–probe spectroscopy study, and analysed the data. H.Y. supervised the fluorescence and pump–probe spectroscopy study, and analysed the data. A.A.-G. supervised the simulation study, and analysed the data. M.B. designed and supervised the overall study, and analysed the data. E.B., N.S. and M.B. wrote the manuscript. J.L.B., R.V. and S.L. edited the manuscript and all authors commented on the manuscript.

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Correspondence to Hao Yan or Alán Aspuru-Guzik or Mark Bathe.

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Boulais, É., Sawaya, N., Veneziano, R. et al. Programmed coherent coupling in a synthetic DNA-based excitonic circuit. Nat. Mater. 17, 159–166 (2018). https://doi.org/10.1038/nmat5033

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