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Programming nanoparticle valence bonds with single-stranded DNA encoders

Abstract

Nature has evolved strategies to encode information within a single biopolymer to program biomolecular interactions with characteristic stoichiometry, orthogonality and reconfigurability. Nevertheless, synthetic approaches for programming molecular reactions or assembly generally rely on the use of multiple polymer chains (for example, patchy particles). Here we demonstrate a method for patterning colloidal gold nanoparticles with valence bond analogues using single-stranded DNA encoders containing polyadenine (polyA). By programming the order, length and sequence of each encoder with alternating polyA/non-polyA domains, we synthesize programmable atom-like nanoparticles (PANs) with n-valence that can be used to assemble a spectrum of low-coordination colloidal molecules with different composition, size, chirality and linearity. Moreover, by exploiting the reconfigurability of PANs, we demonstrate dynamic colloidal bond-breaking and bond-formation reactions, structural rearrangement and even the implementation of Boolean logic operations. This approach may be useful for generating responsive functional materials for distinct technological applications.

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Fig. 1: Programmable atom equivalents fabrication using single-stranded DNA encoders.
Fig. 2: Schematic representation and TEM images of colloidal molecules.
Fig. 3: Schematic illustration and TEM images of colloidal oligomers.
Fig. 4: Colloidal molecules with anisotropy and chirality.
Fig. 5: Programmable colloidal reactions based on atom equivalents.
Fig. 6: Programmable single-particle nanocircuits based on atom equivalents.

Data availability

All the data that support the findings of this study are available within the paper and its Supplementary Information files, and from the corresponding authors upon reasonable request.

References

  1. 1.

    Garzoni, M., Okuro, K., Ishii, N., Aida, T. & Pavan, G. M. Structure and shape effects of molecular glue on supramolecular tubulin assemblies. ACS Nano 8, 904–914 (2014).

    CAS  Article  Google Scholar 

  2. 2.

    Bednar, J. et al. Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher-order folding and compaction of chromatin. Proc. Natl Acad. Sci. USA 95, 14173–14178 (1998).

    CAS  Article  Google Scholar 

  3. 3.

    Lane, T., Serwer, P., Hayes, S. J. & Eiserling, F. Quantized viral-DNA packaging revealed by rotating gel-electrophoresis. Virology 174, 472–478 (1990).

    CAS  Article  Google Scholar 

  4. 4.

    Routh, A., Sandin, S. & Rhodes, D. Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc. Natl Acad. Sci. USA 105, 8872–8877 (2008).

    CAS  Article  Google Scholar 

  5. 5.

    Folsch, S., Martinez-Blanco, J., Yang, J. S., Kanisawa, K. & Erwin, S. C. Quantum dots with single-atom precision. Nat. Nanotechnol. 9, 505–508 (2014).

    Article  CAS  Google Scholar 

  6. 6.

    Chen, J. W. et al. Artificial muscle-like function from hierarchical supramolecular assembly of photoresponsive molecular motors. Nat. Chem. 10, 132–138 (2018).

    CAS  Article  Google Scholar 

  7. 7.

    Zhang, C. et al. A general approach to DNA-programmable atom equivalents. Nat. Mater. 12, 741–746 (2013).

    CAS  Article  Google Scholar 

  8. 8.

    Macfarlane, R. J., O’Brien, M. N., Petrosko, S. H. & Mirkin, C. A. Nucleic acid-modified nanostructures as programmable atom equivalents: forging a new “Table of Elements”. Angew. Chem. Int. Edit. 52, 5688–5698 (2013).

    CAS  Article  Google Scholar 

  9. 9.

    Jones, M. R. et al. DNA-nanoparticle superlattices formed from anisotropic building blocks. Nat. Mater. 9, 913–917 (2010).

    CAS  Article  Google Scholar 

  10. 10.

    Wang, Y. et al. Colloids with valence and specific directional bonding. Nature 491, 51–55 (2012).

    CAS  Article  Google Scholar 

  11. 11.

    Kraft, D. J. et al. Surface roughness directed self-assembly of patchy particles into colloidal micelles. Proc. Natl Acad. Sci. USA 109, 10787–10792 (2012).

    CAS  Article  Google Scholar 

  12. 12.

    Feng, L., Dreyfus, R., Sha, R. J., Seeman, N. C. & Chaikin, P. M. DNA patchy particles. Adv. Mater. 25, 2779–2783 (2013).

    CAS  Article  Google Scholar 

  13. 13.

    Groschel, A. H. et al. Guided hierarchical co-assembly of soft patchy nanoparticles. Nature 503, 247–251 (2013).

    Article  CAS  Google Scholar 

  14. 14.

    Rozynek, Z., Mikkelsen, A., Dommersnes, P. & Fossum, J. O. Electroformation of Janus and patchy capsules. Nat. Commun. 5, 3945 (2014).

    CAS  Article  Google Scholar 

  15. 15.

    Newton, A. C., Groenewold, J., Kegel, W. K. & Bolhuis, P. G. Rotational diffusion affects the dynamical self-assembly pathways of patchy particles. Proc. Natl Acad. Sci. USA 112, 15308–15313 (2015).

    CAS  Article  Google Scholar 

  16. 16.

    Gong, Z., Hueckel, T., Yi, G. R. & Sacanna, S. Patchy particles made by colloidal fusion. Nature 550, 234–238 (2017).

    Article  CAS  Google Scholar 

  17. 17.

    Choueiri, R. M. et al. Surface patterning of nanoparticles with polymer patches. Nature 538, 79–83 (2016).

    CAS  Article  Google Scholar 

  18. 18.

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

    Article  CAS  Google Scholar 

  19. 19.

    Tan, S. J., Campolongo, M. J., Luo, D. & Cheng, W. Building plasmonic nanostructures with DNA. Nat. Nanotechnol. 6, 268–276 (2011).

    CAS  Article  Google Scholar 

  20. 20.

    Liu, W. Y., Halverson, J., Tian, Y., Tkachenko, A. V. & Gang, O. Self-organized architectures from assorted DNA-framed nanoparticles. Nat. Chem. 8, 867–873 (2016).

    CAS  Article  Google Scholar 

  21. 21.

    Li, Y., Liu, Z., Yu, G., Jiang, W. & Mao, C. Self-assembly of molecule-like nanoparticle clusters directed by DNA nanocages. J. Am. Chem. Soc. 137, 4320–4323 (2015).

    CAS  Article  Google Scholar 

  22. 22.

    Alivisatos, A. P. et al. Organization of ‘nanocrystal molecules’ using DNA. Nature 382, 609–611 (1996).

    CAS  Article  Google Scholar 

  23. 23.

    Park, S. Y. et al. DNA-programmable nanoparticle crystallization. Nature 451, 553–556 (2008).

    CAS  Article  Google Scholar 

  24. 24.

    Macfarlane, R. J. et al. Nanoparticle superlattice engineering with DNA. Science 334, 204–208 (2011).

    CAS  Article  Google Scholar 

  25. 25.

    Auyeung, E. et al. DNA-mediated nanoparticle crystallization into wulff polyhedra. Nature 505, 73–77 (2014).

    Article  CAS  Google Scholar 

  26. 26.

    Liu, W. et al. Diamond family of nanoparticle superlattices. Science 351, 582–586 (2016).

    CAS  Article  Google Scholar 

  27. 27.

    Tan, L. H., Xing, H., Chen, H. Y. & Lu, Y. Facile and efficient preparation of anisotropic DNA-functionalized gold nanoparticles and their regioselective assembly. J. Am. Chem. Soc. 135, 17675–17678 (2013).

    CAS  Article  Google Scholar 

  28. 28.

    Xing, H. et al. Bottom-up strategy to prepare nanoparticles with a single DNA strand. J. Am. Chem. Soc. 139, 3623–3626 (2017).

    CAS  Article  Google Scholar 

  29. 29.

    Ben Zion, M. Y. et al. Self-assembled three-dimensional chiral colloidal architecture. Science 358, 633–636 (2017).

    Article  CAS  Google Scholar 

  30. 30.

    Zhang, Y. et al. Transfer of two-dimensional oligonucleotide patterns onto stereocontrolled plasmonic nanostructures through DNA-origami-based nanoimprinting lithography. Angew. Chem. Int. Edit. 55, 8036–8040 (2016).

    CAS  Article  Google Scholar 

  31. 31.

    Edwardson, T. G. W., Lau, K. L., Bousmail, D., Serpell, C. J. & Sleiman, H. F. Transfer of molecular recognition information from DNA nanostructures to gold nanoparticles. Nat. Chem. 8, 162–170 (2016).

    CAS  Article  Google Scholar 

  32. 32.

    Xu, X., Rosi, N. L., Wang, Y., Huo, F. & Mirkin, C. A. Asymmetric functionalization of gold nanoparticles with oligonucleotides. J. Am. Chem. Soc. 128, 9286–9287 (2006).

    CAS  Article  Google Scholar 

  33. 33.

    Huo, F., Lytton-Jean, A. K. R. & Mirkin, C. A. Asymmetric functionalization of nanoparticles based on thermally addressable DNA interconnects. Adv. Mater. 18, 2304–2306 (2006).

    CAS  Article  Google Scholar 

  34. 34.

    Zhang, Y. et al. Selective transformations between nanoparticle superlattices via the reprogramming of DNA-mediated interactions. Nat. Mater. 14, 840–847 (2015).

    CAS  Article  Google Scholar 

  35. 35.

    Kim, Y., Macfarlane, R. J., Jones, M. R. & Mirkin, C. A. Transmutable nanoparticles with reconfigurable surface ligands. Science 351, 579–582 (2016).

    CAS  Article  Google Scholar 

  36. 36.

    Pei, H. et al. Designed diblock oligonucleotide for the synthesis of spatially isolated and highly hybridizable functionalization of DNA-gold nanoparticle banoconjugates. J. Am. Chem. Soc. 134, 11876–11879 (2012).

    CAS  Article  Google Scholar 

  37. 37.

    Yao, G. et al. Clicking DNA to gold nanoparticles: poly-adenine-mediated formation of monovalent DNA-gold nanoparticle conjugates with nearly quantitative yield. NPG Asia Mater. 7, e159 (2015).

    Article  Google Scholar 

  38. 38.

    Fan, J. A. et al. Self-assembled plasmonic nanoparticle clusters. Science 328, 1135–1138 (2010).

    CAS  Article  Google Scholar 

  39. 39.

    Hentschel, M., Schäferling, M., Duan, X., Giessen, H. & Liu, N. Chiral plasmonics. Sci. Adv. 3, e1602735 (2017).

    Article  CAS  Google Scholar 

  40. 40.

    Soloveichik, D., Seelig, G. & Winfree, E. DNA as a universal substrate for chemical kinetics. Proc. Natl Acad. Sci. USA 107, 5393–5398 (2010).

    CAS  Article  Google Scholar 

  41. 41.

    Zhang, D. Y. & Winfree, E. Control of DNA strand displacement kinetics using toehold exchange. J. Am. Chem. Soc. 131, 17303–17314 (2009).

    CAS  Article  Google Scholar 

  42. 42.

    Kotani, S. & Hughes, W. L. Multi-arm junctions for dynamic DNA nanotechnology. J. Am. Chem. Soc. 139, 6363–6368 (2017).

    CAS  Article  Google Scholar 

  43. 43.

    Liu, D. B. et al. Resettable, multi-readout logic gates based on controllably reversible aggregation of gold nanoparticles. Angew. Chem. Int. Edit. 50, 4103–4107 (2011).

    CAS  Article  Google Scholar 

  44. 44.

    Feringa, B. L. The art of building small: from molecular switches to motors (Nobel Lecture). Angew. Chem. Int. Edit. 56, 11060–11078 (2017).

    CAS  Article  Google Scholar 

  45. 45.

    Bruns, C. J. & Stoddart, J. F. The Nature of the Mechanical Bond: from Molecules to Machines (John Wiley & Sons, 2017).

  46. 46.

    Balzani, V., Credi, A. & Venturi, M. Molecular Devices and Machines – A Journey into the Nano World (Wiley-VCH, 2003).

  47. 47.

    Shen, J. et al. Valence-engineering of quantum dots using programmable DNA scaffolds. Angew. Chem. Int. Edit. 56, 16077–16081 (2017).

    CAS  Article  Google Scholar 

  48. 48.

    Zhu, D. et al. Coordination-mediated programmable assembly of unmodified oligonucleotides on plasmonic silver nanoparticles. ACS Appl. Mater. Inter. 7, 11047–11052 (2015).

    CAS  Article  Google Scholar 

  49. 49.

    Zhou, L. et al. DNA-mediated construction of hollow upconversion nanoparticles for protein harvesting and near-infrared light triggered release. Adv. Mater. 26, 2424–2430 (2014).

    CAS  Article  Google Scholar 

  50. 50.

    Cecconello, A., Besteiro, L. V., Govorov, A. O. & Willner, I. Chiroplasmonic DNA-based nanostructures. Nat. Rev. Mater 2, 17039 (2017).

    CAS  Article  Google Scholar 

  51. 51.

    Luk’yanchuk, B. et al. The Fano resonance in plasmonic nanostructures and metamaterials. Nat. Mater. 9, 707–715 (2010).

    Article  CAS  Google Scholar 

  52. 52.

    Urban, M. J. et al. Plasmonic toroidal metamolecules assembled by DNA origami. J. Am. Chem. Soc. 138, 5495–5498 (2016).

    CAS  Article  Google Scholar 

  53. 53.

    Lim, D. K. et al. Highly uniform and reproducible surface-enhanced Raman scattering from DNA-tailorable nanoparticles with 1-nm interior gap. Nat. Nanotechnol. 6, 452–460 (2011).

    CAS  Article  Google Scholar 

  54. 54.

    Hartl, C. et al. Position accuracy of gold nanoparticles on DNA origami structures studied with small-angle X-ray scattering. Nano Lett. 18, 2609–2615 (2018).

    CAS  Article  Google Scholar 

  55. 55.

    Nielsen, S. S. et al. BioXTAS RAW, a software program for high-throughput automated small-angle X-ray scattering data reduction and preliminary analysis. J. Appl. Crystallogr. 42, 959–964 (2009).

    CAS  Article  Google Scholar 

  56. 56.

    M. Doucet et al. SasView v.4.1.2 (SasView, 2017); https://doi.org/10.5281/zenodo.825675.

  57. 57.

    Dobrynin, A. V., Rubinstein, M. & Obukhov, S. P. Cascade of transitions of polyelectrolytes in poor solvents. Macromolecules 29, 2974–2979 (1996).

    CAS  Article  Google Scholar 

  58. 58.

    Case, D. A. et al. The amber biomolecular simulation programs. J. Comput. Chem. 26, 1668–1688 (2005).

    CAS  Article  Google Scholar 

  59. 59.

    Zgarbova, M. et al. Refinement of the sugar-phosphate backbone torsion beta for AMBER force fields improves the description of Z- and B-DNA. J. Chem. Theory Comput. 11, 5723–5736 (2015).

    CAS  Article  Google Scholar 

  60. 60.

    Heinz, H., Lin, T. J., Mishra, R. K. & Emami, F. S. Thermodynamically consistent force fields for the assembly of inorganic, organic, and biological nanostructures: the INTERFACE force field. Langmuir 29, 1754–1765 (2013).

    CAS  Article  Google Scholar 

  61. 61.

    Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926–935 (1983).

    CAS  Article  Google Scholar 

  62. 62.

    Tuckerman, M. E., Liu, Y., Ciccotti, G. & Martyna, G. J. Non-Hamiltonian molecular dynamics: generalizing Hamiltonian phase space principles to non-Hamiltonian systems. J. Chem. Phys. 115, 1678–1702 (2001).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Key R&D Program of China (2016YFA0201200), National Natural Science Foundation of China (21834007, 21675167, 31571014, U1532119, 21775157, 11575278), the National Science Foundation (1531991), China Postdoctoral Science Foundation (2015M580373, 2016T90396), the Open Large Infrastructure Research of the Chinese Academy of Sciences, the LU JIAXI International team programme supported by CAS and the K.C. Wong Education Foundation, Shanghai Jiao Tong University. The authors are also thankful for the staff from BL19U2 beamline of National Facility for Protein Science Shanghai (NFPS) at Shanghai Synchrotron Radiation Facility (SSRF) for assistance during data collection.

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Contributions

C.F. and B.L.F. directed the research. C.F., G.Y. and J.L. conceived the study. G.Y., Q.L. and X.C. performed experiments. R.P.N., D.W., G.Y. and H.Y. performed cryogenic electron microscopy imaging and analysis. F.W. and H.P. performed CD theoretical calculations. Z.Q. performed MD simulations. X.L. and X.C. performed SAXS experiments. Z.G. and H.P. assisted in the preparation of polyA–AuNPs. X.L., X.Z. and L.W. assisted with the TEM imaging. G.Y., J.L., Q.L., B.L.F. and C.F. analysed data and wrote the paper.

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Correspondence to Ben L. Feringa or Chunhai Fan.

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Yao, G., Li, J., Li, Q. et al. Programming nanoparticle valence bonds with single-stranded DNA encoders. Nat. Mater. 19, 781–788 (2020). https://doi.org/10.1038/s41563-019-0549-3

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