Implication of Surface Properties, Bacterial Motility, and Hydrodynamic Conditions on Bacterial Surface Sensing and Their Initial Adhesion

Abstract

Biofilms are structured microbial communities attached to surfaces, which play a significant role in the persistence of biofoulings in both medical and industrial settings. Bacteria in biofilms are mostly embedded in a complex matrix comprised of extracellular polymeric substances that provide mechanical stability and protection against environmental adversities. Once the biofilm is matured, it becomes extremely difficult to kill bacteria or mechanically remove biofilms from solid surfaces. Therefore, interrupting the bacterial surface sensing mechanism and subsequent initial binding process of bacteria to surfaces is essential to effectively prevent biofilm-associated problems. Noting that the process of bacterial adhesion is influenced by many factors, including material surface properties, this review summarizes recent works dedicated to understanding the influences of surface charge, surface wettability, roughness, topography, stiffness, and combination of properties on bacterial adhesion. This review also highlights other factors that are often neglected in bacterial adhesion studies such as bacterial motility and the effect of hydrodynamic flow. Lastly, the present review features recent innovations in nanotechnology-based antifouling systems to engineer new concepts of antibiofilm surfaces.

Keywords: antibiofilm surfaces; bacterial adhesion; bacterial motility; bacterial surface sensing; biofilm formation; hydrodynamics; material properties.

FIGURE 1

Schematic illustration of various surface parameters that influence bacterial adhesion. Bacterial adhesion is governed by diverse surface properties, including surface charge density, wettability, roughness, topography, and stiffness. This diagram describes the major aspect of bacterial response to a single surface parameter.

FIGURE 2

Illustration of the extended DLVO theory. The total interaction energy between the bacterium and a substrate is the sum of the electrostatic double layer interactions, Lifshitz-van der Waals interactions, and acid-base interactions. Each energy component can be either attractive or repulsive depending on the surface properties of the bacterium and substrate in aquatic environmental conditions.

FIGURE 3

Effect of surface topography on bacterial adhesion. (A) E. coli bacteria attached on textured surface of dragonfly wing (a). The Helium ion microscopy image (b) indicate progressive dying stages of E. coli on the dragonfly wing starting with No. 1 where the cell attached to the surface and its membrane deforms, ending with No. 4 where the cell membrane lost its integrity and cell sank into nanopillars. Scale bar is 200 nm. Adapted with permission from Bandara et al. (2017) Bactericidal Effects of Natural Nanotopography of Dragonfly Wing on Escherichia coli. ACS Appl Mater Interfaces 9, 6,746–6,760. Copyright © 2017, American Chemical Society. (B) Comparison of P. aeruginosa adhesion on flat (a) and textured surfaces (b). P. aeruginosa appears to cover a smaller surface area on the textured surface with features in 8 μm range in comparison to the flat surface. Adapted with permission from Chang et al. (2018) Surface Topography Hinders Bacterial Surface Motility. ACS Appl Mater Interfaces 10, 9,225–9,234. Copyright © 2018, American Chemical Society. (C) Adherence of S. epidermidis on flat (a) and rose petal-textured (b) surfaces after 2 h incubation. SEM (a,b) and fluorescence microscopy (c,d) images of S. epidermidis showed a decreased amount of bacterial adhesion on the textured surface. Adapted with permission from Cao et al. (2019) Hierarchical Rose Petal Surfaces Delay the Early-Stage Bacterial Biofilm Growth. Langmuir 35, 14,670–14,680. Copyright © 2019, American Chemical Society.

FIGURE 4

Schematic illustration of bacterial adhesion in response to the superhydrophobic surface. The air entrapment phenomena happened in the presence of increased water contact angle (hydrophobicity), and roughness of the substratum. Reprinted with permission from Pan et al. (2019) Picosecond Laser-Textured Stainless Steel Superhydrophobic Surface with an Antibacterial Adhesion Property. Langmuir 35, 11,414–11,421. Copyright © 2019, American Chemical Society.

FIGURE 5

Schematic illustration of the effects of surface wettability on bacterial adhesion under dynamic conditions. (A) Schematic illustration of S. aureus adhesion on hydrophilic nanopillar surfaces under static and fluid conditions. In the static condition, bacteria adhere to both the nanopillar tips and troughs, while bacteria adhere to only the nanopillar tips under fluid conditions. Adapted from Hizal et al. (2017). (B) Schematic illustration of S. aureus adhesion on hydrophobic nanopillar surfaces under static and fluid conditions. In the static condition, the bacteria float over the entrapped air layer, and bacteria are swept away by fluid flow. Reprinted with permission from Hizal et al. (2017) Nanoengineered Superhydrophobic Surfaces of Aluminum with Extremely Low Bacterial Adhesivity. ACS Appl Mater Interfaces 9, 12,118–12,129. Copyright© 2017, American Chemical Society.