The nature of inherent bactericidal activity: insights from the nanotopology of three species of dragonfly

Abstract

While insect wings are widely recognised as multi-functional, recent work showed that this extends to extensive bactericidal activity brought about by cell deformation and lysis on the wing nanotopology. We now quantitatively show that subtle changes to this topography result in substantial changes in bactericidal activity that are able to span an order of magnitude. Notably, the chemical composition of the lipid nanopillars was seen by XPS and synchrotron FTIR microspectroscopy to be similar across these activity differences. Modelling the interaction between bacterial cells and the wing surface lipids of 3 species of dragonflies, that inhabit similar environments, but with distinctly different behavioural repertoires, provided the relationship between surface structure and antibacterial functionality. In doing so, these principal behavioural patterns correlated with the demands for antimicrobial efficiency dictated by differences in their foraging strategies. This work now reveals a new feature in the design elegance of natural multi-functional surfaces as well providing insights into the bactericidal mechanism underlying inherently antimicrobial materials, while suggesting that nanotopology is related to the evolutionary development of a species through the demands of its behavioural repertoire. The underlying relationship between the processes of wetting, adhesion and capillarity of the lipid nanopillars and bactericidal efficiency suggests new prospects for purely mechano-responsive antibacterial surfaces.

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.…”

“…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.…”

“…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.…”

ZnO Nanopillar Coated Surfaces with Substrate‐Dependent Superbactericidal Property

“…These results indicate that the ZnO nanopillar surface is very efficient in killing adhered bacteria and fungi cells. Although it is known that motile bacteria, such as E. coli and P. aeruginosa are more easily killed by surface nanoarrays with rupturing mechanism,[11a] here, both motile and nonmotile bacteria were killed on ZnO nanopillar surfaces …”

Mechano-bactericidal nanopillars require external forces to effectively kill bacteria

“…Changing the surface chemistry of the cicada wing did not alter antibacterial effectiveness, implying that bactericidal activity of natural nanopillar arrays originates from physical interactions that can deform and rupture the bacterial cell wall 8 . Subsequent studies showed similar nanopillar-induced antibacterial behaviour on the wings of other insects, such as damselflies and dragonflies, which have sharper nanopillars said to deliver even higher antibacterial efficacy [9][10] . These initial discoveries prompted the development of engineered nanopillars capable of mimicking this physical antibacterial mechanism such as black silicon nanopillars that mimic nanopillars of dragonfly wings and have remarkable bactericidal activity 11 .…”