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DNA condensation in one dimension

Abstract

DNA can be programmed to assemble into a variety of shapes and patterns on the nanoscale1,2,3,4,5 and can act as a template for hybrid nanostructures6 such as conducting wires7,8,9, protein arrays8 and field-effect transistors10,11. Current DNA nanostructures are typically in the sub-micrometre range, limited by the sequence space and length of the assembled strands. Here we show that on a patterned biochip12, DNA chains collapse into one-dimensional (1D) fibres that are 20 nm wide and around 70 µm long, each comprising approximately 35 co-aligned chains at its cross-section. Electron beam writing on a photocleavable monolayer was used to immobilize and pattern the DNA molecules, which condense into 1D bundles in the presence of spermidine. DNA condensation can propagate and split at junctions, cross gaps and create domain walls between counterpropagating fronts. This system is inherently adept at solving probabilistic problems and was used to find the possible paths through a maze and to evaluate stochastic switching circuits. This technique could be used to propagate biological or ionic signals13 in combination with sequence-specific DNA nanotechnology or for gene expression in cell-free DNA compartments14.

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Figure 1: Assembly and structure of nanobundles.
Figure 2: Structural properties of nuclei and 1D bundles.
Figure 3: Front propagation dynamics.
Figure 4: Condensation through a graphical representation of a maze.
Figure 5: 1D DNA condensation bridges over gap barriers.

References

  1. 1

    Seeman, N. C. Nanomaterials based on DNA. Annu. Rev. Biochem. 79, 65–87 (2010).

    CAS  Article  Google Scholar 

  2. 2

    Jones, M. R., Seeman, N. C. & Mirkin, C. A. Programmable materials and the nature of the DNA bond. Science 347, 1260901 (2015).

    Article  Google Scholar 

  3. 3

    Rothemund, P. W. K. Folding DNA to create nanoscale shapes and patterns. Nature 440, 297–302 (2006).

    CAS  Article  Google Scholar 

  4. 4

    Ke, Y. et al. DNA brick crystals with prescribed depths. Nature Chem. 6, 994–1002 (2014).

    CAS  Article  Google Scholar 

  5. 5

    Catherall, T., Huskisson, D., McAdams, S. & Vijayaraghavan, A. Self-assembly of one dimensional DNA-templated structures. J. Mater. Chem. C 2, 6895–6920 (2014).

    CAS  Article  Google Scholar 

  6. 6

    Bui, H. et al. Programmable periodicity of quantum dot arrays with DNA origami nanotubes. Nano Lett. 10, 3367–3372 (2010).

    CAS  Article  Google Scholar 

  7. 7

    Braun, E., Eichen, Y., Sivan, U. & Ben-Yoseph, G. DNA-templated assembly and electrode attachment of a conducting silver wire. Nature 391, 775–778 (1998).

    CAS  Article  Google Scholar 

  8. 8

    Yan, H., Park, S. H., Finkelstein, G., Reif, J. H. & LaBean, T. H. DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science 301, 1882–1884 (2003).

    CAS  Article  Google Scholar 

  9. 9

    Liu, J. et al. Fabrication of DNA-templated Te and Bi2Te3 nanowires by galvanic displacement. Langmuir 29, 11176–11184 (2013).

    CAS  Article  Google Scholar 

  10. 10

    Keren, K., Berman, R. S., Buchstab, E., Sivan, U. & Braun, E. DNA-templated carbon nanotube field-effect transistor. Science 302, 1380–1382 (2003).

    CAS  Article  Google Scholar 

  11. 11

    Maune, H. T. et al. Self-assembly of carbon nanotubes into two-dimensional geometries using DNA origami templates. Nature Nanotech. 5, 61–66 (2009).

    Article  Google Scholar 

  12. 12

    Heyman, Y., Buxboim, A., Wolf, S. G., Daube, S. S. & Bar-Ziv, R. H. Cell-free protein synthesis and assembly on a biochip. Nature Nanotech. 7, 374–378 (2012).

    CAS  Article  Google Scholar 

  13. 13

    Berson, J. et al. Single-layer ionic conduction on carboxyl-terminated silane monolayers patterned by constructive lithography. Nature Mater. 14, 613–621 (2015).

    CAS  Article  Google Scholar 

  14. 14

    Karzbrun, E., Tayar, A. M., Noireaux, V. & Bar-Ziv, R. H. Programmable on-chip DNA compartments as artificial cells. Science 345, 829–832 (2014).

    CAS  Article  Google Scholar 

  15. 15

    Hud, N. V. & Vilfan, I. D. Toroidal DNA condensates: unraveling the fine structure and the role of nucleation in determining size. Annu. Rev. Biophys. Biomol. Struct. 34, 295–318 (2005).

    CAS  Article  Google Scholar 

  16. 16

    Pelta, J. Jr, Durand, D., Doucet, J. & Livolant, F. DNA mesophases induced by spermidine: structural properties and biological implications. Biophys. J. 71, 48–63 (1996).

    CAS  Article  Google Scholar 

  17. 17

    Livolant, F. Ordered phases of DNA in vivo and in vitro. Phys. A 176, 117–137 (1991).

    CAS  Article  Google Scholar 

  18. 18

    Yoshikawa, K., Kidoaki, S., Takahashi, M., Vasilevskaya, V. V. & Khokhlov, A. R. Marked discreteness on the coil-globule transition of single duplex DNA. Berich. Bunsen. Gesell. 100, 876–880 (1996).

    CAS  Article  Google Scholar 

  19. 19

    Iwataki, T., Kidoaki, S., Sakaue, T., Yoshikawa, K. & Abramchuk, S. S. Competition between compaction of single chains and bundling of multiple chains in giant DNA molecules. J. Chem. Phys. 120, 4004–4011 (2004).

    CAS  Article  Google Scholar 

  20. 20

    Mel'nikov, S. M., Sergeyev, V. G. & Yoshikawa, K. Discrete coil-globule transition of large DNA induced by cationic surfactant. J. Am. Chem. Soc. 117, 2401–2408 (1995).

    CAS  Article  Google Scholar 

  21. 21

    Petrov, A. S. & Harvey, S. C. Packaging double-helical DNA into viral capsids: structures, forces, and energetics. Biophys. J. 95, 497–502 (2008).

    CAS  Article  Google Scholar 

  22. 22

    Koltover, I., Wagner, K. & Safinya, C. R. DNA condensation in two dimensions. Proc. Natl Acad. Sci. USA 97, 14046–14051 (2000).

    CAS  Article  Google Scholar 

  23. 23

    Bracha, D. & Bar-Ziv, R. H. Dendritic and nanowire assemblies of condensed DNA polymer brushes. J. Am. Chem. Soc. 136, 4945–4953 (2014).

    CAS  Article  Google Scholar 

  24. 24

    Buxboim, A. et al. A single-step photolithographic interface for cell-free gene expression and active biochips. Small 3, 500–510 (2007).

    CAS  Article  Google Scholar 

  25. 25

    Buxboim, A., Daube, S. S. & Bar-Ziv, R. H. Synthetic gene brushes: a structure-function relationship. Mol. Syst. Biol. 4, 181 (2008).

    Article  Google Scholar 

  26. 26

    Bracha, D., Karzbrun, E., Daube, S. S. & Bar-Ziv, R. H. Emergent properties of dense DNA phases toward artificial biosystems on a surface. Acc. Chem. Res. 47, 1912–1921 (2014).

    CAS  Article  Google Scholar 

  27. 27

    Kolodziej, C. M. & Maynard, H. D. Electron-beam lithography for patterning biomolecules at the micron and nanometer scale. Chem. Mater. 24, 774–780 (2012).

    CAS  Article  Google Scholar 

  28. 28

    Bracha, D., Karzbrun, E., Shemer, G., Pincus, P. A. & Bar-Ziv, R. H. Entropy-driven collective interactions in DNA brushes on a biochip. Proc. Natl Acad. Sci. USA 110, 4534–4538 (2013).

    CAS  Article  Google Scholar 

  29. 29

    Hud, N. V. & Downing, K. H. Cryoelectron microscopy of lambda phage DNA condensates in vitreous ice: the fine structure of DNA toroids. Proc. Natl Acad. Sci. USA 98, 14925–14930 (2001).

    CAS  Article  Google Scholar 

  30. 30

    Cohen, H. et al. Polarizability of G4-DNA observed by electrostatic force microscopy measurements. Nano Lett. 7, 981986 (2007).

    Article  Google Scholar 

  31. 31

    Wilhelm, D. & Bruck, J. Stochastic switching circuit synthesis. In 2008 IEEE International Symposium on Information Theory 1388–1392 (IEEE, 2008).

  32. 32

    Tsumoto, K., Luckel, F. & Yoshikawa, K. Giant DNA molecules exhibit on/off switching of transcriptional activity through conformational transition. Biophys. Chem. 106, 23–29 (2003).

    CAS  Article  Google Scholar 

  33. 33

    Estévez-Torres, A. et al. Sequence-independent and reversible photocontrol of transcription/expression systems using a photosensitive nucleic acid binder. Proc. Natl Acad. Sci. USA 106, 12219–12223 (2009).

    Article  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge financial support by the Volkswagen Stiftung (G.P., F.C.S. and R.H.B.-Z., grant no. 86 395), the Israel Science Foundation (R.H.B.-Z.) and the Minerva Foundation (R.H.B.-Z).

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G.P., D.B., F.C.S. and R.H.B.-Z. planned and designed the experiments. G.P., D.B. and O.V. performed the experiments. G.P., D.B., S.S.D., F.C.S. and R.H.B.-Z. wrote the paper; all authors discussed the results and commented on the manuscript.

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Correspondence to Friedrich C. Simmel or Roy H. Bar-Ziv.

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The authors declare no competing financial interests.

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Pardatscher, G., Bracha, D., Daube, S. et al. DNA condensation in one dimension. Nature Nanotech 11, 1076–1081 (2016). https://doi.org/10.1038/nnano.2016.142

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