Surface-associated bacterial communities, known as biofilms, are responsible for a broad spectrum of infections in humans. Recent studies have indicated that surfaces containing nanoscale protrusions, like those in dragonfly wings, create a hostile niche for bacterial colonization and biofilm growth. This functionality has been mimicked on metals and semiconductors by creating nanopillars and other high aspect ratio nanostructures at the interface of these materials. However, bactericidal topographies have not been reported on clinically relevant hydrogels and highly compliant polymers, mostly because of the complexity of fabricating nanopatterns in hydrogels with precise control of the size that can also resist aqueous immersion. Here, we report the fabrication of bioinspired bactericidal nanostructures in bacterial cellulose (BC) hydrogels using low-energy ion beam irradiation. By challenging the currently accepted view, we show that the nanostructures grown in BC affect preferentially stiff membranes like those of the Gram-positive bacteria Bacillus subtilis in a time-dependent manner and, to a lesser extent, the more deformable and softer membrane of Escherichia coli. Moreover, the nanostructures in BC did not affect the viability of murine preosteoblasts. Using single-cell analysis, we demonstrate that indeed B. subtilis requires less force than E. coli to be penetrated by nanoprobes with dimensions comparable to those of the nanostructured BC, providing the first direct experimental evidence validating a mechanical model of membrane rupture via a tension-induced mechanism within the activation energy theory. Our findings bridge the gap between mechano-bactericidal surfaces and low-dimensional materials, including single-walled carbon nanotubes and graphene nanosheets, in which a higher bactericidal activity toward Gram-positive bacteria has been extensively reported. Our results also demonstrate the ability to confer bactericidal properties to a hydrogel by only altering its topography at the nanoscale and contribute to a better understanding of the bacterial mechanobiology, which is fundamental for the rational design bactericidal topographies.
Hydrogels provide a solution-mimicking environment for the interaction with living systems that make them desirable for various biomedical and technological applications. Because relevant biological processes in living tissues occur at the biomolecular scale, hydrogel nanopatterning can be leveraged to attain novel material properties and functionalities. However, the fabrication of high aspect ratio (HAR) nanostructures in hydrogels capable of self-standing in aqueous environments, with fine control of the size and shape distribution, remains challenging. Here, we report the synthesis of nanostructures with a HAR in bacterial cellulose (BC) hydrogel via directed plasma nanosynthesis using argon ions. The nanostructures in BC are reproducible, stable to sterilization, and liquid immersion. Using in-situ surface characterization and semiempirical modeling, we discovered that pattern formation was linked to the formation of graphitelike clusters composed of a mixture of C-C and C=C bonds. Moreover, our model predicts that reactive species at the onset of the argon irradiation accelerate the bond breaking of weak bonds, contributing to the formation of an amorphous carbon layer and nanopattern growth.
Bacterial adhesion and biofilm formation on the surface of biomedical devices is a detrimental process that compromises patient safety and material functionality. Several physicochemical factors are involved in biofilm growth, including the surface properties. Among those, material stiffness has recently been suggested to influence microbial adhesion and biofilm growth in a variety of polymers and hydrogels. However, no clear consensus exists about the role of material stiffness on biofilm initiation and whether very compliant substrates are deleterious to bacterial cell adhesion. Here, by systematically tuning substrate topography and stiffness while keeping the surface free energy of polydimethylsiloxane substrates constant, we show that topographical patterns at the micron and submicron scale impart unique properties to the surface that are independent of the material stiffness. The current work provides a better understanding of the role of material stiffness on bacterial physiology and may constitute a cost-effective and simple strategy to reduce bacterial attachment and biofilm growth even in very compliant and hydrophobic polymers.
Device-associated infections are one of the deadliest complications accompanying the use of biomaterials, and despite recent advances in the development of anti-biofouling strategies, biomaterials that exhibit both functional tissue restoration and antimicrobial activity have been challenging to achieve. Here, we report the fabrication of bio-inspired bactericidal nanospikes in bacterial cellulose and investigate the mechanism underlying this phenomenon. We demonstrate these structures affects preferentially stiff membranes like those in Gram-positive bacteria, but exhibit cytocompatibility towards mammalian cells, a requisite for tissue restoration. We also reveal the bactericidal activity of the nanospikes is due to a pressure-induced mechanism, which depends on the cell's adherence time, nanospike's geometry and spacing, cell shape, and mechanical properties of the cell wall. Our findings provide a better understanding of the mechanobiology of bacterial cells at the interface with nanoscale structures, which is fundamental for the rational design bactericidal topographies.
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