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A dissipative pathway for the structural evolution of DNA fibres

Abstract

Biochemical networks interconnect, grow and evolve to express new properties as different chemical pathways are selected during a continuous cycle of energy consumption and transformation. In contrast, synthetic systems that push away from equilibrium usually return to the same self-assembled state, often generating waste that limits system recyclability and prevents the formation of adaptable networks. Here we show that annealing by slow proton dissipation selects for otherwise inaccessible morphologies of fibres built from DNA and cyanuric acid. Using single-molecule fluorescence microscopy, we observe that proton dissipation influences the growth mechanism of supramolecular polymerization, healing gaps within fibres and converting highly branched, interwoven networks into nanocable superstructures. Just as the growth kinetics of natural fibres determine their structural attributes to modulate function, our system of photoacid-enabled depolymerization and repolymerization selects for healed materials to yield organized, robust fibres. Our method provides a chemical route for error-checking, distinct from thermal annealing, that improves the morphologies and properties of supramolecular materials using out-of-equilibrium systems.

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Fig. 1: A light-activated cycle of proton dissipation to regulate the assembly of fibre states.
Fig. 2: Proton dissipation switches the assembly mechanism of DNA fibres at the single-molecule level: TIRF-M investigation.
Fig. 3: Backfilling of short DNA strands into individual A30–CA fibres to determine fibre homogeneity.
Fig. 4: Hierarchical assembly of A30–CA before and after proton dissipation.
Fig. 5: Cryo-EM images of A30–CA fibres before and after proton dissipation.

Data availability

All data supporting the findings of this study are available in the main text or the supplementary materials.

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Acknowledgements

G.C. and H.F.S. are grateful to the National Science and Engineering Research Council of Canada (NSERC), the Canada Foundation for Innovation (CFI), and the Fonds de Recherche Nature et Technologies (FRQNT). H.F.S. is also grateful to the Canada Research Chairs Program, the Canada Council for the Arts for a Killam Fellowship, and is a Cottrell Scholar of the Research Corporation. A.G. thanks the Canada Institute for Health Research (CIHR) and the McGill Facility for Electron Microscopy Research (FEMR). F.J.R., C.M.P and C.L.-B. thank NSERC for a Banting Fellowship, CGS-D Scholarship, and Vanier Scholarship, respectively. The authors thank Y. Gidi for insightful discussions on the single-molecule data.

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F.J.R, C.M.P. and H.F.S. conceived and designed the experiments. F.J.R. and H.F.S. performed and analysed the ensemble experiments. C.M.P. and G.C. conceived, performed and analysed the single-molecule fluorescence experiments. X.L. and M.D.D. performed the AFM experiments. C.L.-B. performed the persistence length analyses. Y.S. and A.G. performed and analysed the cryo-EM experiments. F.J.R, C.M.P. and H.F.S. co-wrote the paper with input from all authors.

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Correspondence to Hanadi F. Sleiman.

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Peer review information Nature Chemistry thanks Subi George, Mathieu Surin and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Rizzuto, F.J., Platnich, C.M., Luo, X. et al. A dissipative pathway for the structural evolution of DNA fibres. Nat. Chem. 13, 843–849 (2021). https://doi.org/10.1038/s41557-021-00751-w

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