Bioinspired, Dynamic, Structured Surfaces for Biofilm Prevention

Abstract

Bacteria primarily exist in robust, surface-associated communities known as biofilms, ubiquitous in both natural and anthropogenic environments. Mature biofilms resist a wide range of biocidal treatments and pose persistent pathogenic threats. Treatment of adherent biofilm is difficult, costly, and, in medical systems such as catheters, frequently impossible. Adding to the challenge, we have discovered that biofilm can be both impenetrable to vapors and extremely nonwetting, repelling even low surface tension commercial antimicrobials. Our study shows multiple contributing factors, including biochemical components and multiscale reentrant topography. Reliant on surface chemistry, conventional strategies for preventing biofilm only transiently affect attachment and/or are environmentally toxic. In this work, we look to Nature’s antifouling solutions, such as the dynamic spiny skin of the echinoderm, and we develop a versatile surface nanofabrication platform. Our benchtop approach unites soft lithography, electrodeposition, mold deformation, and material selection to enable many degrees of freedom—material, geometric, mechanical, dynamic—that can be programmed starting from a single master structure. The mechanical properties of the bio-inspired nanostructures, verified by AFM, are precisely and rationally tunable. We examine how synthetic dynamic nanostructured surfaces control the attachment of pathogenic biofilms. The parameters governing long-range patterning of bacteria on high-aspect-ratio (HAR) nanoarrays are combinatorially elucidated, and we discover that sufficiently low effective stiffness of these HAR arrays mechanoselectively inhibits ~40% of Pseudomonas aeruginosa biofilm attachment. Inspired by the active echinoderm skin, we design and fabricate externally actuated dynamic elastomer surfaces with active surface microtopography. We extract from a large parameter space the critical topographic length scales and actuation time scales for achieving nearly ~80% attachment reduction. We furthermore investigate an atomically mobile, slippery liquid infused porous surface (SLIPS) inspired by the pitcher plant. We show up to 99.6% reduction of multiple pathogenic biofilms over a 7-day period under both static and physiologically realistic flow conditions—a ~35x improvement over state-of-the-art surface chemistry, and over a far longer timeframe. Moreover, SLIPS is shown to be nontoxic: bacteria simply cannot attach to the smooth liquid interface. These bio-inspired strategies significantly advance biofilm attachment prevention and promise a tremendous range of industrial, clinical, and consumer applications.