Spatial distribution of mechanical properties in Pseudomonas aeruginosa biofilms, and their potential impacts on biofilm deformation

Abstract

The mechanical properties of biofilms can be used to predict biofilm deformation under external forces, for example, under fluid flow. We used magnetic tweezers to spatially map the compliance of Pseudomonas aeruginosa biofilms at the microscale, then applied modeling to assess its effects on biofilm deformation. Biofilms were grown in capillary flow cells with Reynolds numbers (Re) ranging from 0.28 to 13.9, bulk dissolved oxygen (DO) concentrations from 1 mg/L to 8 mg/L, and bulk calcium ion (Ca2+) concentrations of 0 and 100 mg CaCl2/L. Higher Re numbers resulted in more uniform biofilm morphologies. The biofilm was stiffer at the center of the flow cell than near the walls. Lower bulk DO led to more stratified biofilms. Higher Ca2+ concentrations led to increased stiffness and more uniform mechanical properties. Using the experimental mechanical properties, fluid–structure interaction models predicted up to 64% greater deformation for heterogeneous biofilms, compared with a homogeneous biofilms with the same average properties. However, the deviation depended on the biofilm morphology and flow regime. Our results show significant spatial mechanical variability exists at the microscale, and that this variability can potentially affect biofilm deformation. The average biofilm mechanical properties, provided in many studies, should be used with caution when predicting biofilm deformation.

Data‐driven modeling of heterogeneous viscoelastic biofilms

“…In previous studies (Galy et al, 2012; Pavissich et al, 2021), biofilm mechanical properties, including Young's modulus and viscosity, differed up by as much as two orders of magnitude within the same biofilm. Therefore, in this study we assumed the non‐Newtonian viscosity varied between 100 and 1100 Pa·s.…”

“…In previous studies (Galy et al, 2012;Pavissich et al, 2021), biofilm mechanical properties, including Young's modulus and…”

“…Only a few studies have addressed the structural and mechanical heterogeneity of biofilms. In recent years, microscale techniques, including atomic force microscopy (AFM) and microrheological techniques, have been developed and applied in biofilm studies (Cao et al, 2016; Galy et al, 2012; Pavissich et al, 2021; Volle et al, 2008). However, these methods are limited.…”

Effects of biofilm heterogeneity on the apparent mechanical properties obtained by shear rheometry

“…Stress sweep tests were performed to identify the LVR for all three types of agar biofilms, and the rheometer analyses used in this study were all within the LVR. While large deformations may capture the nonlinear region of viscoelasticity (Charlton et al, 2019;Jana et al, 2020;Li et al, 2020Li et al, , 2021Xia et al, 2022), we chose to avoid this mechanical behavior to simplify our analyses.…”

“…Consolidation occurs in the deeper biofilm, leading to a denser and stiffer biofilm interior (Laspidou & Rittmann, 2004). Chemical gradients of oxygen and nutrients can further stratify the local mechanical heterogeneity in the biofilm (Pavissich et al, 2021;P. S. Stewart & Franklin, 2008).…”