Mechanical Resilience of Biofilms toward Environmental Perturbations Mediated by Extracellular Matrix

• Published in: Advanced functional materials Vol. 32; no. 23
• Main Authors: Zhang, Qiuting, Nguyen, Danh, Tai, Jung‐Shen B., Xu, XJ, Nijjer, Japinder, Huang, Xin, Li, Ying, Yan, Jing
• Format: Journal Article
• Language: English
• Published: Hoboken Wiley Subscription Services, Inc 01.06.2022
• Subjects: Biofilms; environmental perturbations; Extracellular matrix; Materials science; Mechanics (physics); Molecular dynamics; nonlinear viscoelasticity; Perturbation; Resilience; Rheological properties; Rheology; Shear forces; soft materials; Viscoelastic materials; Viscoelasticity
• ISSN: 1616-301X; 1616-3028
• DOI: 10.1002/adfm.202110699

Biofilms are surface‐associated communities of bacterial cells embedded in an extracellular matrix (ECM). Biofilm cells can survive and thrive in various dynamic environments causing tenacious problems in healthcare and industry. From a materials science point of view, biofilms can be considered as soft, viscoelastic materials, and exhibit remarkable mechanical resilience. How biofilms achieve such resilience toward various environmental perturbations remain unclear, although ECM has been generally considered to play a key role. Here, Vibrio cholerae (Vc) is used as a model organism to investigate biofilm mechanics in the nonlinear rheological regime by systematically examining the role of each constituent matrix component. Combining mutagenesis, rheological measurements, and molecular dynamics simulations, the mechanical behaviors of various mutant biofilms and their distinct mechanical phenotypes including mechanics‐guided morphologies, nonlinear viscoelastic behavior, and recovery from large shear forces and heating are investigated. The results show that the ECM polymeric network protects the embedded cells from environmental challenges by providing mechanical resilience in response to large mechanical perturbation. The findings provide physical insights into the structure–property relationship of biofilms, which can be potentially employed to design biofilm removal strategies or, more forward‐looking, engineer biofilms as beneficial, functional soft materials in dynamic environments. Bacterial biofilms cause tenacious problems in healthcare and industry in various dynamic environments. Combing mutagenesis, rheological characterization, and molecular dynamics simulations, it is demonstrated how extracellular polysaccharides, proteins, and cells function together to define the mechanical behavior of Vibrio cholerae biofilm, including mechano‐morphogenesis, nonlinear viscoelastic behavior, and mechanical resilience under large shear forces and heating.