Fluid‐driven interfacial instabilities and turbulence in bacterial biofilms

Abstract

Summary Biofilms are thin layers of bacteria embedded within a slime matrix that live on surfaces. They are ubiquitous in nature and responsible for many medical and dental infections, industrial fouling and are also evident in ancient fossils. A biofilm structure is shaped by growth, detachment and response to mechanical forces acting on them. The main contribution to biofilm versatility in response to physical forces is the matrix that provides a platform for the bacteria to grow. The interaction between biofilm structure and hydrodynamics remains a fundamental question concerning biofilm dynamics. Here, we document the appearance of ripples and wrinkles in biofilms grown from three species of bacteria when subjected to high‐velocity fluid flows. Linear stability analysis suggested that the ripples were Kelvin–Helmholtz Instabilities. The analysis also predicted a strong dependence of the instability formation on biofilm viscosity explaining the different surface corrugations observed. Turbulence through Kelvin–Helmholtz instabilities occurring at the interface demonstrated that the biofilm flows like a viscous liquid under high flow velocities applied within milliseconds. Biofilm fluid‐like behavior may have important implications for our understanding of how fluid flow influences biofilm biology since turbulence will likely disrupt metabolite and signal gradients as well as community stratification.

Computational and Experimental Investigation of Biofilm Disruption Dynamics Induced by High-Velocity Gas Jet Impingement

“…Here, there was no evidence that the biofilm structure was expanded during impingement. Finally, although biofilm grown from a single species was analyzed here, the literature shows remarkable similarity in the viscoelastic responses of many different types of biofilms when subject to shear stresses, even though the magnitude of the elastic and viscous moduli vary over many orders of magnitude (42); thus, it is reasonable to conclude that biofilms formed from other species might exhibit flow behavior similar to that described here, as suggested by the ripple patterns experimentally observed in Pseudomonas aeruginosa and Staphylococcus epidermidis biofilms exposed to high-velocity shear flows (3).…”

“…The amphiphilic character and surfactant production are associated as main effects controlling surface tension in microbial colonies and biofilms (45,46), being attributed the surface tension reduction due to the presence of surfactants (36,39,45). Biofilm surface tension differences could also explain the different ripple patterns observed between S. mutans biofilms and biofilms grown from Pseudomonas aeruginosa and Staphylococcus epidermidis (3). A lower surface tension intensified the formation of small-amplitude waves near the impact zone (i.e., the more "flexible" interface was more wrinkled).…”

“…D uring recent years, close attention has been paid to the mechanical behavior of biofilms when subjected to high shear turbulent flows, because of direct applications in utilizing such methods for biofilm removal. Fluid-biofilm patterns, such as formation of migratory ripples and surface instabilities, transition to fluid-like behavior, and stretching to finally break off the biofilm, have been described (1)(2)(3)(4)(5). Furthermore, the viscoelastic character of biofilms when exposed to turbulent flows has been reported (6)(7)(8), hypothesizing that generated instabilities enhance mass transfer into biofilms (9,10).…”

“…Small biofilm deformations have also been modeled considering the biofilm as a poroelastic material, compressing when exposed to laminar flows (20,21). The effect of parallel air-water jets on the surface morphology of very viscous biofilms has been investigated numerically (3,22), proposing the characterization of the biofilm rippling as Kelvin-Helmholtz instability. However, the interactions between biofilm and perpendicular impinging turbulent jet flow and how the turbulent impacts disrupt biofilm properties have not yet been described numerically.…”

Reduction in Pseudomonas aeruginosa and Staphylococcus aureus biofilms from implant materials in a diffusion dominated environment

“…However, our system, like many in vitro models, did not have the presence of a host response that might be able to eradicate the remaining bacteria once the antibiotics had killed most of the biofilm bacteria. Although complete removal was not observed, the approximate seven log reduction seen across materials and both strains after 24 h could have potentially disrupted the biofilm mechanism and structure, allowing antibiotics to have greater physical access to bacteria, as has been seen in dental biofilms . Ongoing work to collect infected surgical explants from revision surgeries and study their interactions with antibiotic‐loaded CS‐B exposure will expand knowledge of their ability to eradicate biofilms in vivo.…”