Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces

Abstract

The nanopattern on the surface of Clanger cicada (Psaltoda claripennis) wings represents the first example of a new class of biomaterials that can kill bacteria on contact based solely on their physical surface structure. The wings provide a model for the development of novel functional surfaces that possess an increased resistance to bacterial contamination and infection. We propose a biophysical model of the interactions between bacterial cells and cicada wing surface structures, and show that mechanical properties, in particular cell rigidity, are key factors in determining bacterial resistance/sensitivity to the bactericidal nature of the wing surface. We confirmed this experimentally by decreasing the rigidity of surface-resistant strains through microwave irradiation of the cells, which renders them susceptible to the wing effects. Our findings demonstrate the potential benefits of incorporating cicada wing nanopatterns into the design of antibacterial nanomaterials.

Figure 1

Cicada (P. claripennis) wing surface topography. (a) Scanning electron micrograph of the surface of a cicada wing as viewed from above (scale bar = 200 nm). (b) Three-dimensional representation of the surface architecture of a cicada wing, constructed from AFM scan data and colored according to height. A three-dimensional animation of the cicada wing surface is available at http://youtu.be/JDOEAUdqJGk.

Figure 2

Biophysical model of the interactions between cicada (P. claripennis) wing nanopillars and bacterial cells. (a) Schematic of a bacterial outer layer adsorbing onto cicada wing nanopillars. The adsorbed layer can be divided into two regions: region A (in contact with the pillars) and region B (suspended between the pillars). Because region A adsorbs and the surface area of the region (S_A) increases, region B is stretched and eventually ruptures. (b–e) Three-dimensional representation of the modeled interactions between a rod-shaped cell and the wing surface. As the cell comes into contact (b) and adsorbs onto the nanopillars (c), the outer layer begins to rupture in the regions between the pillars (d) and collapses onto the surface (e). Images b–e are screenshots from an animation of the mechanism available at http://youtu.be/KSdMYX4gqp8.

Figure 3

Modeled stretching dynamics of the outer layer of a bacterial cell in contact with a cicada wing surface. (a) Stretching in region A (α_A, dashed lines) and region B (α_B, solid lines) is plotted as a function of the layer parameter ζ for layers under different degrees of initial stretching (α_i), denoted by color. (b) Stretching in α_A and α_B is plotted as a function of the position of the layer relative to junction point M between the spherical cap and conical base of the nanopillars. Both α_A and α_B are plotted for different combinations of ζ and α_i. The equilibrium position of the layer in each case is marked with a dot.

Figure 4

Cell interactions of surface-resistant B. subtilis NCIMB 3610T, Planococcus maritimus KMM 3738, and S. aureus CIP 65.8T strains after MW irradiation. All three strains were rendered susceptible to the action of the wing surface by MW treatment. Typical scanning electron micrographs (left) show substantial deformation of the cell morphologies of all three species. A CLSM viability analysis (right) shows that all cells were inactivated (shown in red).