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Deep-hole transfer leads to ultrafast charge migration in DNA hairpins

Nature Chemistry volume 8, pages 1015–1021 (2016)Cite this article

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Abstract

Charge transport through the DNA double helix is of fundamental interest in chemistry and biochemistry, but also has potential technological applications such as for DNA-based nanoelectronics. For the latter, it is of considerable interest to explore ways to influence or enhance charge transfer. In this Article we demonstrate a new mechanism for DNA charge transport, namely ‘deep-hole transfer’, which involves long-range migration of a hole through low-lying electronic states of the nucleobases. Here, we demonstrate, in a combined experimental and theoretical study, that it is possible to achieve such transfer behaviour by changing the energetics of charge injection. This mechanism leads to an enhancement in transfer rates by up to two orders of magnitude and much weaker distance dependence. This transfer is faster than relaxation to the lowest-energy state, setting this mechanism apart from those previously described. This opens up a new direction to optimize charge transfer in DNA with unprecedented charge-transfer rates.

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Figure 1: Structures and energetics of molecular fragments.
Figure 2: Femtosecond transient spectra of the hairpins.
Figure 3: Comparison of the rate constants for charge separation obtained for NDI–An–SD and SA–An–SD hairpins.
Figure 4: Model system for hole transfer simulations, where four propagating states and one trap state are considered for each adenine.
Figure 5: Simulated hole dynamics in NDI–A3–SD.

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Acknowledgements

This material is based on work supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division under award no. DE-FG02-96ER14604 (F.D.L.) and the US Office of Naval Research MURI grant no. N00014-11-1-0729 (M.R.W., Y.A.B. and M.A.R.). The research leading to these results has received funding from the European Research Council FP7 ERC grant agreement no. 240299 and Horizon 2020 ERC grant agreement no. 648433.

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Author notes

  1. Nicolas Renaud, Michelle A. Harris and Arunoday P. N. Singh: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Chemical Engineering, Delft University of Technology, 2628 BL, Delft, The Netherlands

    Nicolas Renaud & Ferdinand C. Grozema

  2. Department of Chemistry, Northwestern University, Evanston, 60208-3113, Illinois, USA

    Michelle A. Harris, Arunoday P. N. Singh, Yuri A. Berlin, Mark A. Ratner, Michael R. Wasielewski & Frederick D. Lewis

  3. Argonne-Northwestern Solar Energy Research (ANSER) Center, Northwestern University, Evanston, 60208-3113, Illinois, USA.

    Michelle A. Harris, Mark A. Ratner & Michael R. Wasielewski

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Contributions

A.P.N.S. and F.D.L. synthesized the DNA hairpins and performed structural characterization. M.A.H. and M.R.W. conceived and performed the transient absorption spectroscopy as well as the global analysis of the results. N.R., Y.A.B., M.A.R. and F.C.G. developed the model and performed the theoretical calculations. N.R., F.D.L. and F.C.G. wrote the paper with contributions from all authors.

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Correspondence to Michael R. Wasielewski, Frederick D. Lewis or Ferdinand C. Grozema.

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The authors declare no competing financial interests.

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Renaud, N., Harris, M., Singh, A. et al. Deep-hole transfer leads to ultrafast charge migration in DNA hairpins. Nature Chem 8, 1015–1021 (2016). https://doi.org/10.1038/nchem.2590

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