Self-assembly of nanoparticles into biomimetic capsid-like nanoshells

Journal name:
Nature Chemistry
Volume:
9,
Pages:
287–294
Year published:
DOI:
doi:10.1038/nchem.2641
Received
Accepted
Published online

Abstract

Nanoscale compartments are one of the foundational elements of living systems. Capsids, carboxysomes, exosomes, vacuoles and other nanoshells easily self-assemble from biomolecules such as lipids or proteins, but not from inorganic nanomaterials because of difficulties with the replication of spherical tiling. Here we show that stabilizer-free polydispersed inorganic nanoparticles (NPs) can spontaneously organize into porous nanoshells. The association of water-soluble CdS NPs into self-limited spherical capsules is the result of scale-modified electrostatic, dispersion and other colloidal forces. They cannot be accurately described by the Derjaguin–Landau–Vervey–Overbeek theory, whereas molecular-dynamics simulations with combined atomistic and coarse-grained description of NPs reveal the emergence of nanoshells and some of their stabilization mechanisms. Morphology of the simulated assemblies formed under different conditions matched nearly perfectly the transmission electron microscopy tomography data. This study bridges the gap between biological and inorganic self-assembling nanosystems and conceptualizes a new pathway to spontaneous compartmentalization for a wide range of inorganic NPs including those existing on prebiotic Earth.

At a glance

Figures

  1. Nanoshells spontaneously form from ‘naked’ polydispersed inorganic NPs.
    Figure 1: Nanoshells spontaneously form from ‘naked’ polydispersed inorganic NPs.

    a, A TEM image of CdS nanoshells (22 ± 4 nm) obtained at pH 9.5. These nanoshells share similarities with capsids, but consist of small inorganic NPs (3–5 nm) without apparent structural anisotropy, precise molecular tiling and specific lock-and-key interaction. b, A high-resolution TEM image of a CdS nanoshell shows the packing of the constituent NPs on the surface; the thickness of the nanoshell corresponds to a monolayer of NPs. c, A high-resolution TEM image of several nanoshells showing crystal lattices of (111) planes of cubic CdS. d, The enlarged high-resolution image of the area in the white rectangle in c that can be associated with the constituent NP tetrahedron.

  2. 3D structure of nanoshells from CdS NPs obtained by TEM tomography.
    Figure 2: 3D structure of nanoshells from CdS NPs obtained by TEM tomography.

    ad, Surface (a,c) and cross-section (b,d) of the nanoshell at room temperature (a,b) and at cryo-conditions (c,d), capturing the structural information of the assemblies in their native environment and showing the porous nature of the nanoshells. e, 3D surface rendering of the nanoshell with differently coloured NP domains without any special geometric fit. 3D reconstruction of the nanoshells is also given in the Supplementary Movie 3.

  3. Temporal progression and intermediate stages of nanoshell assembly that demonstrate the gradual transition from individual NPs to nanoshells.
    Figure 3: Temporal progression and intermediate stages of nanoshell assembly that demonstrate the gradual transition from individual NPs to nanoshells.

    Representative TEM images of CdS nanoshells obtained after the assembly at pH 9.5. a,b, The presence of individual NPs with the emergence of embryonic forms of nanoshells at 5 min. c,d, Arc-shaped assemblies as an intermediate precursor for nanoshells appear at 10 min. e,f, After 20 min complete shells are formed.

  4. Model 1 MD simulation of NP self-organization with high atomic precision but short effective assembly times.
    Figure 4: Model 1 MD simulation of NP self-organization with high atomic precision but short effective assembly times.

    ac, Snapshots taken after ~65 ns simulations of assemblies from NPs that carry q = 0.3e (a), 0.9e (b) and 1.34e (c). Yellow–green units represent individual NPs. Other colours denote assembled NP particles with different degrees of connectivity. Sodium counterions are shown as yellow spheres. Note the extended assemblies from multiple connected particles (red, orange and yellow) that mirror the arc-shaped structures in Fig. 3c,d. d, Atomic charges on the NP surfaces and in the cores were calculated with ab initio methods using small atomic clusters. e, Snapshot after ~22 ns equilibration for pre-assembled NPs that carry q = 0.9e. Inset shows an enlarged view of the highlighted region; note the atomistic description of both the surface and media. f, Plots for the number of water molecules inside the nanoshells with q = 0.3e, 0.6e and 0.9e. Stabilization of the cavity size for q = 0.3e and 0.6e is indicative of stabilization of the shell in a (local) thermodynamic minimum.

  5. Model 2 and Model 3 MD simulations of NP self-organization with progressive coarse graining and longer effective assembly times.
    Figure 5: Model 2 and Model 3 MD simulations of NP self-organization with progressive coarse graining and longer effective assembly times.

    ad, Surface representation of the pre-assembled nanoshells taken from simulations after ~1 ns equilibration time (translucent green) and after ~85 ns equilibration time (red) for NPs in Model 2 carrying net effective charges of q = 0e (a), 2e (b), 4e (c) and 8e (d). The yellow lines mark the artificially formed fixed opening made to accelerate the exchange of water and ions and observe longer effective assembly times. The lower images show the corresponding cross-sections of the nanoshells. Sodium counter ions are shown by yellow spheres. Note the close similarity with TEM images in Fig. 1 and tomography data in Fig. 2. e,f, Plots of the number of water molecules (e) and percent of ions (f) inside the nanoshells in Model 2. A gradual stabilization of the number of water molecules, and thus the cavity size, is observed (Supplementary Fig. 11 gives the distribution of these ions). gj, Surface of Model 3 nanoshells for NPs with q = 0e (g), 0.6e (h), 1e (i) and 2e (j). The translucent green shades show the initial pre-assembled nanoshells, whereas the red images show simulated structures taken from ~33 ns simulations. The nanoshells with values of Model 3 effective charge q higher than 1e destabilize due to electrostatic repulsion of NPs.

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Author information

Affiliations

  1. Department of Chemical Engineering, University of Michigan, Ann Arbor, Michigan 48109, USA

    • Ming Yang &
    • Nicholas A. Kotov
  2. Biointerfaces Institute, University of Michigan, Ann Arbor, Michigan 48109, USA

    • Ming Yang,
    • Joong Hwan Bahng &
    • Nicholas A. Kotov
  3. Key Laboratory of Microsystems and Micronanostructures Manufacturing, Harbin Institute of Technology, Harbin 150080, China

    • Ming Yang
  4. Department of Chemistry, University of Illinois in Chicago, Chicago, Illinois 60607, USA

    • Henry Chan &
    • Petr Král
  5. Department of Structural Biology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15260, USA

    • Gongpu Zhao &
    • Peijun Zhang
  6. Department of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan 48109, USA

    • Joong Hwan Bahng &
    • Nicholas A. Kotov
  7. Department of Mechanical Engineering and Materials Science, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, Pennsylvania 15260, USA

    • Peijun Zhang
  8. Department of Physics, University of Illinois in Chicago, Chicago, Illinois 60607, USA

    • Petr Král
  9. Department of Biopharmaceutical Sciences, University of Illinois in Chicago, Chicago, Illinois 60612, USA

    • Petr Král
  10. Department of Material Sciences and Engineering, University of Michigan, Ann Arbor, Michigan 48109, USA

    • Nicholas A. Kotov
  11. Michigan Center for Integrative Research in Critical Care, Ann Arbor, Michigan 48109, USA

    • Nicholas A. Kotov

Contributions

M.Y. performed the experiments, conceived the DLVO theory model and analysed the data. H.C. and P.K conceived the Gauss model and performed the MD simulations. G.Z. and P.Z. carried out and analysed the TEM tomography study. J.H.B. contributed the dynamic light-scattering experiments and calculations of the surface potential/charge of the NPs. N.A.K. conceived the project and designed the study. M.Y., H.C., P.K., G.Z., P.Z. and N.A.K. co-wrote the paper.

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The authors declare no competing financial interests.

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