Bacterial Biofilm Material Properties Enable Removal and Transfer by Capillary Peeling

Abstract

Biofilms, surface-attached communities of bacterial cells, are a concern in health and in industrial operations because of persistent infections, clogging of flows, and surface fouling. Extracellular matrices provide mechanical protection to biofilm-dwelling cells as well as protection from chemical insults, including antibiotics. Understanding how biofilm material properties arise from constituent matrix components and how these properties change in different environments is crucial for designing biofilm removal strategies. Here, using rheological characterization and surface analyses of Vibrio cholerae biofilms, we discover how extracellular polysaccharides, proteins, and cells function together to define biofilm mechanical and interfacial properties. Using insight gained from our measurements, we develop a facile capillary peeling technology to remove biofilms from surfaces or to transfer intact biofilms from one surface to another. We show that our findings are applicable to other biofilm-forming bacterial species and to multiple surfaces. Thus, our technology and the '( ) ! e p ' !

Microstructural and Rheological Transitions in Bacterial Biofilms

“…Weak strain overshoots have been frequently reported in colloidal glasses/gels [ 43 ] and have also been observed in biofilms of Pseudomonas aeruginosa , Bacillus subtilis , and Vibrio cholerae . [ 11,16 ] In contrast, the WT strain was devoid of weak strain overshoots and had $$G^{^{\prime \prime }}(\gamma )$$ behavior indicative of strain thinning that has been commonly seen in viscoelastic liquids and polymer melts. [ 43 ]…”

“…For example, certain extracellular proteins and eDNA can cross-link the ECM, whilst general ECM secretion creates osmotic gradients, driving colony expansion and increasing cell-cell distances. [16,[18][19][20] However, a clear understanding of the relationship between biofilm viscoelastic behavior and structure as a function of ECM composition is yet to be thoroughly explored. [21] Conceptually, the presence of bacterial cells (dispersed phase), ECM (continuous phase), and the interactions between the two phases within a biofilm make it structurally similar to polymercolloidal mixtures.…”

“…[11,13,25,34] This route has been used to study the influence of ECM composition on biofilm structure or rheology. [16,35] Yet, the relationship between packing fraction and biofilm viscoelasticity as a function of ECM secretion, remains largely unknown. [14,21] Here, we investigated the viscoelastic response of a biofilm system due to changes in its exopolysaccharide production.…”

“…[ 12 , 13 , 14 , 15 ] Biofilm viscoelastic response is modulated by structural components of ECM which, in turn, influence its structural properties, such as cell ordering and packing. [ 11 , 16 , 17 ] The structural components impart physical functions to the ECM. For example, certain extracellular proteins and eDNA can cross‐link the ECM, whilst general ECM secretion creates osmotic gradients, driving colony expansion and increasing cell–cell distances.…”

“…For example, certain extracellular proteins and eDNA can cross‐link the ECM, whilst general ECM secretion creates osmotic gradients, driving colony expansion and increasing cell–cell distances. [ 16 , 18 , 19 , 20 ] However, a clear understanding of the relationship between biofilm viscoelastic behavior and structure as a function of ECM composition is yet to be thoroughly explored. [ 21 ]…”