How rigid are viruses

Viruses have traditionally been studied as pathogens, but in recent years they have been adapted for applications ranging from drug delivery and gene therapy to nanotechnology, photonics, and electronics. Although the structures of many viruses are known, most of their biophysical properties remain largely unexplored. Using Brillouin light scattering, we analyzed the mechanical rigidity, intervirion coupling, and vibrational eigenmodes of Wiseana iridovirus (WIV). We identified phonon modes propagating through the viral assemblies as well as the localized vibrational eigenmode of individual viruses. The measurements indicate a Young’s modulus of $\sim 7\mathrm{GPa}$ for single virus particles and their assemblies, surprisingly high for “soft” materials. Mechanical modeling confirms that the DNA core dominates the WIV rigidity. The results also indicate a peculiar mechanical coupling during self-assembly of WIV particles.

Figure 1

Electron microscopy images of Wiseana Iridovirus (WIV) samples. (a) Transmission electron microscopy image of a single WIV showing the compact DNA core (dark) and the surrounding protein shell. Scanning electron micrographs of (b) scattered single viruses, (c) single-layer of disordered viruses, and (d) expanded view of a single layer showing disordered packing of WIV virions.

Figure 2

Scanning electron micrograph of PMMA colloids $(D=300\mathrm{nm})$ on an aluminum mirror.

Figure 3

(Color online) A representative volume element of matrix embedded with a spherical WIV having a DNA core and a capsid shell and its finite element meshes.

Figure 4

(Color online) Brillouin scattering spectra at different scattering wave vectors. (a) Spectra of a layer of PMMA colloids measured at $Q=14\mu {\mathrm{m}}^{-1}$ (thick blue line) and at $Q=20\mu {\mathrm{m}}^{-1}$ (thin red line), no analyzer used. $Q$-independent peaks indicate vibrational modes localized to individual particles. (b) Spectra of a layer of PMMA colloids measured at $Q=6.3\mu {\mathrm{m}}^{-1}$ polarized (thick blue line) and depolarized (thin red line). The rise of the intensity at frequencies above $\sim 10\mathrm{GHz}$ in the polarized spectrum is the tail of longitudinal acousticlike modes localized inside of PMMA particles. (c) Spectra of a multilayered WIV sample measured at $Q=14\mu {\mathrm{m}}^{-1}$ (thick blue line) and at $Q=20\mu {\mathrm{m}}^{-1}$ (thin red line), no analyzer used. $Q$-dependent peaks indicate vibrational modes propagating in the film of the viruses. The lowest-frequency mode (marked by letter $R$) is the Rayleigh mode. Other modes are higher-order Sezawa modes.

Figure 5

(Color online) Brillouin scattering spectra of thin WIV structures, no analyzer used. The spectra on each figure are shifted vertically for clarity: (a) Spectra of a single layer of WIV measured at $Q=14\mu {\mathrm{m}}^{-1}$ (top spectrum), $Q=20\mu {\mathrm{m}}^{-1}$ (middle spectrum) and $Q=24\mu {\mathrm{m}}^{-1}$ (lower spectrum). Weak modes exhibit some $Q$ dependence. (b) Spectra of a single layer of WIV measured at $Q=17\mu {\mathrm{m}}^{-1}$ (top spectrum) and $Q=20\mu {\mathrm{m}}^{-1}$ (lower spectrum). A weak $Q$-independent mode is visible near $9\mathrm{GHz}$. (c) Spectra of a submonolayer of WIV [Fig. 1b] measured at $Q=20\mu {\mathrm{m}}^{-1}$ (top spectrum) and $Q=24\mu {\mathrm{m}}^{-1}$ (middle spectrum) also exhibit $Q$-independent mode near $9\mathrm{GHz}$. The strong peaks at higher frequency are surface Rayleigh mode of Si. Spectrum of Si substrate (lower spectrum) is shown for comparison.

Figure 6

(Color online) Frequency of Brillouin modes in WIV spectra as a function of the scattering wave vector $Q$. $Q$-independent modes are interpreted as localized vibrations from single-layer (open squares) and submonolayer (open circles) WIV assemblies. The average frequency of the localized mode ($8.8\pm 0.2\mathrm{GHz}$, marked by a solid line) was used in Eq. (3) to estimate transverse sound velocity. $Q$-dependent modes are propagating surface waves from multilayer WIV structures (solid squares). $R$ marks the Rayleigh mode and $S$ marks the first-order Sezawa mode. The solid line represents the asymptotic value of the Rayleigh velocity at high $Q$. Error bars represent one standard deviation from averaging positive and negative Brillouin frequency shifts.

Figure 7

(Color online) Effective bulk modulus of the whole WIV particle $k^{*}$ predicted by an analytic solution (ROM) and a numerical method (FEM) assuming different values for the Young’s modulus of DNA, $E_D$.