Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Spontaneous assembly of viruses on multilayered polymer surfaces

Nature Materials volume 5, pages 234–240 (2006)Cite this article

Abstract

The idea that randomly arranged supermolecular species incorporated in a network medium can ultimately create ordered structures at the surface may be counterintuitive. However, such order can be accommodated by regulating dynamic and equilibrium driving forces. Here, we present the ordering of M13 viruses, highly complex biomacromolecules, driven by competitive electrostatic binding, preferential macromolecular interactions and the rigid-rod nature of the virus systems during alternating electrostatic assembly. The steric constraints inherent to the competitive charge binding between M13 viruses and two oppositely charged weak polyelectrolytes leads to interdiffusion and the virtual ‘floating’ of viruses to the surface. The result is the spontaneous formation of a two-dimensional monolayer structure of viruses atop a cohesive polyelectrolyte multilayer. We demonstrate that this viral-assembled monolayer can be a biologically tunable scaffold to nucleate, grow and align nanoparticles or nanowires over multiple length scales. This system represents an interface that provides a general platform for the systematic incorporation and assembly of organic, biological and inorganic materials.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Materials used in this study.
Figure 2: A schematic strategy of the viral monolayer assembly and an AFM demonstration of the disordered state and the ordered monolayer state of the M13 virus.
Figure 3: A series of images to investigate the interdiffusion process in the LPEI/PAA system.
Figure 4: Density control in an electrostatically regulated viral monolayer.
Figure 5: Demonstration of templated biomineralization on the virus monolayer.

Similar content being viewed by others

References

  1. Whitesides, G. M. & Grzybowski, B. Self-assembly at all scales. Science 295, 2418–2421 (2002).

    Article  Google Scholar 

  2. Shinbrot, T. & Muzzio, F. J. Noise to order. Nature 410, 251–258 (2001).

    Article  Google Scholar 

  3. Ball, P. The Self-Made Tapestry: Pattern Formation in Nature (Oxford Univ. Press, New York, 2001).

    Google Scholar 

  4. Hatgerink, J. D., Beniash, E. & Stupp, S. I. Self-assembly and mineralization of peptide-amphiphile nanofibers. Science 294, 1684–1688 (2001).

    Article  Google Scholar 

  5. Park, S., Lim, J. H., Chung, S. W. & Mirkin, C. A. Self-assembly of mesoscopic metal-polymer amphiphiles. Science 303, 348–351 (2004).

    Article  Google Scholar 

  6. Bates, F. S. & Fredrickson, G. H. Block copolymers—Designer soft materials. Phys. Today 52, 32–38 (1999).

    Article  Google Scholar 

  7. Bowden, N., Terfort, A., Carbeck, J. & Whitesides, G. M. Self-assembly of mesoscale objects into ordered two-dimensional arrays. Science 276, 233–235 (1997).

    Article  Google Scholar 

  8. Jaeger, H. M., Nagel, S. R. & Behringer, R. P. Granular solids, liquids, and gases. Rev. Mod. Phys. 68, 1259–1273 (1996).

    Article  Google Scholar 

  9. Möbius, M. E., Lauderdale, B. E., Nagel, S. R. & Jaeger, H. M. Size separation of granular particles. Nature 414, 270 (2001).

    Article  Google Scholar 

  10. Gordon, M. J., Huang, X., Pentoney, S. L. & Zare, R. N. Capillary elctrophoresis. Science 242, 224–228 (1988).

    Article  Google Scholar 

  11. Han, J. & Craighead, H. G. Separation of long DNA molecules in a microfabricated entropic trap array. Science 288, 1026–1029 (2000).

    Article  Google Scholar 

  12. Niemayer, C. M. Nanoparticles, proteins, and nucleic acids: Biotechnology meets materials science. Angew. Chem. Int. Edn 22, 4128–4158 (2001).

    Article  Google Scholar 

  13. Whitesides, G. M., Mathias, J. P. & Seto, C. T. Molecular self-assembly and nanochemistry: A chemical strategy for the synthesis of nanostructures. Science 254, 1312–1319 (1991).

    Article  Google Scholar 

  14. Decher, G. Fuzzy nanoassemblies: Toward layered polymeric multicomposites. Science 277, 1232–1237 (1997).

    Article  Google Scholar 

  15. Caruso, F., Caruso, R. A. & Möhwald, H. Nanoengineering of inorganic and hybrid hollow spheres by colloidal templating. Science 282, 1111–1114 (1998).

    Article  Google Scholar 

  16. Tang, Z., Kotov, N. A., Magonov, S. & Ozturk, B. Nanostructured artificial nacre. Nature Mater. 2, 413–418 (2003).

    Article  Google Scholar 

  17. Hammond, P. T. Form and funtion in multilayer assembly: New applications at the nanoscale. Adv. Mater. 16, 1271–1293 (2004).

    Article  Google Scholar 

  18. De Smedt, S. C., Demeester, J. & Hennink, W. E. Cationic polymer based gene delivery systems. Pharm. Res. 17, 113–126 (2000).

    Article  Google Scholar 

  19. DeLongchamp, D. M. & Hammond, P. T. Fast ion conduction in layer-by-layer polymer films. Chem. Mater. 15, 1165–1173 (2003).

    Article  Google Scholar 

  20. Picart, C. et al. Molecular basis for the explanation of the exponential growth of polyelectrolyte multilayers. Proc. Natl Acad. Sci. USA 99, 12531–12535 (2002).

    Article  Google Scholar 

  21. Lavalle, P. et al. Comparison of the structure of polyelectrolyte multilayer films exhibiting a linear and an exponential growth regime: An in situ atomic force microscopy study. Macromolecules 35, 4458–4465 (2002).

    Article  Google Scholar 

  22. Adams, M., Dogic, Z., Keller, S. L. & Fraden, S. Entropically driven microphase transitions in mixtures of colloidal rods and spheres. Nature 393, 349–352 (1998).

    Article  Google Scholar 

  23. Lee, S. W., Mao, C., Flynn, C. E. & Belcher, A. M. Ordering of quantum dots using genetically engineered viruses. Science 296, 892–895 (2002).

    Article  Google Scholar 

  24. Mao, C. et al. Virus-based toolkit for the directed synthesis of magnetic and semiconducting nanowires. Science 303, 213–217 (2004).

    Article  Google Scholar 

  25. Huang, Y. et al. Programmable assembly of nanoarchitectures using genetically engineered viruses. Nano Lett. 5, 1429–1434 (2005).

    Article  Google Scholar 

  26. Whang, D., Jin, S., Wu, Y. & Lieber, C. M. Large-scale hierarchical organization of nanowire arrays for integrated nanosystems. Nano Lett. 3, 1255–1259 (2003).

    Article  Google Scholar 

  27. Yang, P. Wires on water. Nature 425, 243–244 (2003).

    Article  Google Scholar 

  28. Purdy, K. R. & Fraden, S. Isotropic-cholesteric phase transition of filamentous virus suspensions as a function of rod length and charge. Phys. Rev. E 70, 061703 (2004).

    Article  Google Scholar 

  29. Zimmermann, K., Hagedorn, H., Heuck, C. C., Hinrichsen, M. & Ludwig, H. The ionic properties of the filamentous bacteriophages Pf1 and fd. J. Biol. Chem. 261, 1653–1655 (1996).

    Google Scholar 

  30. Mészáros, R., Thompson, L., Bos, M. & de Groot, P. Adsorption and electrokinetic properties of polyethylenimine on silica surfaces. Langmuir 18, 6164–6169 (2002).

    Article  Google Scholar 

  31. Russell, T. P. et al. Direct observation of reptation at polymer interfaces. Nature 365, 235–237 (1993).

    Article  Google Scholar 

  32. Herzfeld, J. Entropically driven order in crowded solutions: From liquid crystals to cell biology. Acc. Chem. Res. 29, 31–37 (1996).

    Article  Google Scholar 

  33. Dogic, Z. & Fraden, S. Smectic phase in a colloidal suspensions of semiflexible virus particles. Phys. Rev. Lett. 78, 2417–2420 (1997).

    Article  Google Scholar 

  34. Rädler, J. O., Koltover, I., Salditt, T. & Safinya, C. R. Structure of DNA-cationic liposome complexes: DNA interaction in multilamellar membranes in distinct interhelical packing regimes. Science 275, 810–814 (1997).

    Article  Google Scholar 

  35. Borukhov, I., Bruinsma, R. F., Gelbart, W. M. & Liu, A. J. Structural polymorphism of the cytoskeleton: A model of linker-assisted filament aggregation. Proc. Natl Acad. Sci. USA 102, 3673–3678 (2005).

    Article  Google Scholar 

  36. Brand, H. R., Cladis, P. E. & Pleiner, H. Symmetry and defects in the CM phase of polymeric liquid crystals. Macromolecules 25, 7223–7226 (1992).

    Article  Google Scholar 

  37. Warner, M. G. & Hutchinson, J. E. Linear assemblies of nanoparticles electrostatically organized on DNA scaffolds. Nature Mater. 2, 272–277 (2003).

    Article  Google Scholar 

  38. Mann, S. et al. Crystallization at inorganic-organic interfaces: Biominerals and biomimetic synthesis. Science 261, 1286–1292 (1993).

    Article  Google Scholar 

  39. Murr, M. M. & Morse, D. E. Fractal intermediates in the self-assembly of silicatein filaments. Proc. Natl Acad. Sci. USA 102, 11657–11662 (2005).

    Article  Google Scholar 

  40. Whaley, S. R., English, D. S., Hu, E. L., Barbara, P. F. & Belcher, A. M. Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly. Nature 405, 665–668 (2000).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Army Research Office Institute of Soldier Nanotechnologies, The Institute of Collaborative Biotechnologies, and a joint DSO ATO DARPA grant. We thank S. T. Kottmann and A. S. Khalil for the computer graphic work in Fig. 1b. We also thank F. Frankel for her support and assistance in the development of images for this article.

Author information

Author notes

  1. Pil J. Yoo and Ki Tae Nam: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139, USA

    Pil J. Yoo & Paula T. Hammond

  2. Institute for Soldier Nanotechnologies, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139, USA

    Pil J. Yoo, Ki Tae Nam, Angela M. Belcher & Paula T. Hammond

  3. Department of Materials Science and Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139, USA

    Ki Tae Nam, Jifa Qi, Juhyun Park & Angela M. Belcher

  4. Biological Engineering Division, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139, USA

    Jifa Qi, Soo-Kwan Lee & Angela M. Belcher

Authors
  1. Pil J. Yoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ki Tae Nam
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jifa Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Soo-Kwan Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juhyun Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Angela M. Belcher
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Paula T. Hammond
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Angela M. Belcher or Paula T. Hammond.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yoo, P., Nam, K., Qi, J. et al. Spontaneous assembly of viruses on multilayered polymer surfaces. Nature Mater 5, 234–240 (2006). https://doi.org/10.1038/nmat1596

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nmat1596

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing