Bactericidal Effects of Natural Nanotopography of Dragonfly Wing on Escherichia coli

Abstract

Nanotextured surfaces (NTSs) are critical to organisms as self-adaptation and survival tools. These NTSs have been actively mimicked in the process of developing bactericidal surfaces for diverse biomedical and hygiene applications. To design and fabricate bactericidal topographies effectively for various applications, understanding the bactericidal mechanism of NTS in nature is essential. The current mechanistic explanations on natural bactericidal activity of nanopillars have not utilized recent advances in microscopy to study the natural interaction. This research reveals the natural bactericidal interaction between E. coli and a dragonfly wing's (Orthetrum villosovittatum) NTS using advanced microscopy techniques and proposes a model. Contrary to the existing mechanistic models, this experimental approach demonstrated that the NTS of Orthetrum villosovittatum dragonfly wings has two prominent nanopillar populations and the resolved interface shows membrane damage occurred without direct contact of the bacterial cell membrane with the nanopillars. We propose that the bacterial membrane damage is initiated by a combination of strong adhesion between nanopillars and bacterium EPS layer as well as shear force when immobilized bacterium attempts to move on the NTS. These findings could help guide the design of novel biomimetic nanomaterials by maximizing the synergies between biochemical and mechanical bactericidal effects.

Multi-directional electrodeposited gold nanospikes for antibacterial surface applications

“…The inter-pillar spacing on the substrata used in this study was slightly larger than that of a number of previously reported effective antibacterial surfaces, which would initially suggest that nanofeature height plays an important role in the overall bactericidal behaviour of the substrates. This assertion has been oen speculated and reported in the relevant literature for both experimental 23,[32][33][34]46,49 and theoretical studies 22,38 of naturally occurring and biomimetic antibacterial nanostructures. These studies have also shown that the modication of various surface parameters can signicantly alter the bactericidal activity of the surface.…”

“…20,22,[24][25][26]31,32,[34][35][36]38,[53][54][55][56][57] While the precise mechanism responsible for the antibacterial activity is still the subject of debate, 32,58 the consensus between the results obtained from both experimental [22][23][24][25][26]31,32,38,59,60 and theoretical 32,33 studies suggest that a torsional force is induced across the bacterial membrane upon surface adsorption.…”

“…The smaller, more-rigid, spherical S. aureus cells have a higher probability of attaching in these non-lethal regions than the larger P. aeruginosa cells. These multi-directional, bimodal nanostructures may exhibit a greater biocidal activity than that of the more regular nanostructures previously investigated, including both naturally occuring 23,25,26,32,[34][35][36][53][54][55] and synthetic 24,27,33,37,48,49,54,57,65 surfaces. This occurs because the bacteria are subjected to forces operating in multiple directions during surface adsorption, which limits their ability to evade critical membrane damage, and hence cell death.…”

High‐Aspect‐Ratio Nanostructured Surfaces as Biological Metamaterials

“…Others have suggested that membrane rupture occurs not during settling, but when cells attempt to move about on the surface. The argument is that cells are so strongly adhered to the nanostructures, they lyse themselves while trying to move . Researchers investigating titanium‐based nanostructures have suggested that rather than membrane rupture, the surface inhibits membrane remodeling after cell division.…”

Antibacterial activity on superhydrophobic titania nanotube arrays

“…[17–20] These surfaces are typically fabricated either by covalently attaching molecules with low surface energies to a roughened surface or by roughening the surface of a material which is already hydrophobic. [7,17,21,22] Such surfaces are of interest for a diverse array of applications.…”