Nature-Inspired Micro/Nano-Structured Antibacterial Surfaces

Abstract

The problem of bacterial resistance has become more and more common with improvements in health care. Worryingly, the misuse of antibiotics leads to an increase in bacterial multidrug resistance and the development of new antibiotics has virtually stalled. These challenges have prompted the need to combat bacterial infections with the use of radically different approaches. Taking lessons from the exciting properties of micro-/nano-natural-patterned surfaces, which can destroy cellular integrity, the construction of artificial surfaces to mimic natural functions provides new opportunities for the innovation and development of biomedicine. Due to the diversity of natural surfaces, functional surfaces inspired by natural surfaces have a wide range of applications in healthcare. Nature-inspired surface structures have emerged as an effective and durable strategy to prevent bacterial infection, opening a new way to alleviate the problem of bacterial drug resistance. The present situation of bactericidal and antifouling surfaces with natural and biomimetic micro-/nano-structures is briefly reviewed. In addition, these innovative nature-inspired methods are used to manufacture a variety of artificial surfaces to achieve extraordinary antibacterial properties. In particular, the physical antibacterial effect of nature-inspired surfaces and the functional mechanisms of chemical groups, small molecules, and ions are discussed, as well as the wide current and future applications of artificial biomimetic micro-/nano-surfaces. Current challenges and future development directions are also discussed at the end. In the future, controlling the use of micro-/nano-structures and their subsequent functions will lead to biomimetic surfaces offering great potential applications in biomedicine.

Keywords: antibacterial surfaces; bioinspired; biomimetic; micro-/nano-structured.

Figure 1

(A,B) Scanning electron microscope (SEM) micrographs of the upper (frontal) surface of Dahlia flower leaf (petal) under different treatments [13]. (C,D) Bark bugs of different sizes, (E) camouflage of dried animals on dried bark; (F) camouflage of dry animals on wet bark; (G) camouflage of wet animals on wet bark; (H) camouflage of wet animals on dry bark [15]. (I) Photograph of the gecko Lucasium steindachneri; (J) the microstructure of the outer skin of the gecko abdomen and (K) the microstructure of the dorsal area of the gecko; (L) topographical SEM image of the epidermal dome regions and areas between scales on the dorsal region of the lizard; (M–O) micro-/nano-structure of dorsal scales of gecko [17].

Figure 2

Bionic micro-/nano-structures on the surface of the analog. SEM images: (A) moth-eye imaging of simulated terrain [45]; (B) Escherichia coli interacts with the black silicon surface, scale bars 500 nm [46]; (C) hooked polystyrene films based on three-dimensional nanopyramids [48]; (D) cone-shaped nano-structures fabricated using electron beam induced deposition technology [49]; (E) dagger-like structure of zeolitic imidazolate framework coatings on glass (circled in red box) [39]; (F,G) spherical and hemispheric allylamine plasma polymer coatings on glass [43].

Figure 3

Three-dimensional schematic diagram of simulated interaction between rod-shaped bacteria model and cicada wing. As the cell comes into contact (a) and adsorbs onto the nanopillars (b), the outer layer begins to rupture in the regions between the pillars (c) and collapses onto the surface (d) [26].

Figure 4

(A) TEM micrographs showing bacteria–nanopillar interaction at the interface. (a) Longitudinal section of Escherichia coli bacterium approached on two tall nanopillars of a dragonfly wing topography. The membrane is still intact and is pressed inward. A nanoscale space between bacterial membrane and nanopillars can be noted (#). This pseudo-nanospace is filled by EPS; therefore bacterium is physically attached to the nanopillars via EPS layer. As EPS does not have sufficient contrast to the surrounding under TEM, we do not see EPS as a separate layer in the image. Bending of the nanopillars underneath the bacterium is highlighted by the green dashed lines. (b) Longitudinal cross section showing a separation of the inner membrane (IM) and outer membrane (OM) at the polar ends of the Escherichia coli bacterium. The tall nanopillars are bent underneath the bacterium. (c) Longitudinal cross section of a bacterium on the dragonfly wing. Bent tall nanopillars are highlighted by white arrow heads. Small gap between nanopillars and the bacterial membrane is still observed (space between red and blue lines, #). Increased membrane separation at the polar end of the bacterium is present. All scale bars correspond to 200 nm. (B) Proposed mechanism of bactericidal activity of nanopillars. The mechanism of bactericidal activity based on current accepted mechanistic models using cicada wing structure is shown in (a–d). The proposed mechanism based on the experimental studies in this work (using dragonfly wing) is shown in (e–h). (a) Cross section of a cicada wing was used for the current studies to determine bactericidal activity. All nanopillars are assumed to be the same in height. (b) A bacterium approaches on the surface, and the membrane starts to compress due to weight and adsorption. (c) The membrane starts to rupture between attached nanopillars due to stretching. The energy for stretching and membrane deformation is provided by the initial adsorption. (d) Once cell membrane ruptures, the bacterium’s cytoplasm leaks, leading to cell death on the nanopillar surface. (e) Illustration of the dragonfly wing’s two prominent nanopillar populations. (f) Once bacteria approach to the surface, taller nanopillars are being bent by the bacterium. The nanopillars do not puncture the membrane. Bacterium adheres to the nanopillars by the secreted EPS layer and the pilus structures. Once adhesive forces apply stress on bacterial membrane, the two cell membranes of the bacterium start to separate from each other (indicated by the arrow). The EPS layer is displayed in blue, the outer membrane in dark red, and the inner membrane in yellow. (g) The damaged bacterial membrane starts wrinkling and forms blebs (arrows), with separation of the nanopillar layer from the wing base, also observable due to the attempts made by the bacterium to move away. (h) Once the bacteria die on nanopillars, cytosol is leaked and flows under the nanopillar layer filling the crack formed in the previous step. Nanopillars can be seen inside the bacterium at this stage.