Nonlinear rheological characteristics of single species bacterial biofilms

Saikat Jana,J Grant Burgess,Thomas P Curtis,Jinju Chen,Anil Wipat,Samuel G V Charlton,Lucy E Eland

doi:10.1038/s41522-020-0126-1

Abstract

Bacterial biofilms in natural and artificial environments perform a wide array of beneficial or detrimental functions and exhibit resistance to physical as well as chemical perturbations. In dynamic environments, where periodic or aperiodic flows over surfaces are involved, biofilms can be subjected to large shear forces. The ability to withstand these forces, which is often attributed to the resilience of the extracellular matrix. This attribute of the extracellular matrix is referred to as viscoelasticity and is a result of self-assembly and cross-linking of multiple polymeric components that are secreted by the microbes. We aim to understand the viscoelastic characteristic of biofilms subjected to large shear forces by performing Large Amplitude Oscillatory Shear (LAOS) experiments on four species of bacterial biofilms: Bacillus subtilis, Comamonas denitrificans, Pseudomonas fluorescens and Pseudomonas aeruginosa. We find that nonlinear viscoelastic measures such as intracycle strain stiffening and intracycle shear thickening for each of the tested species, exhibit subtle or distinct differences in the plot of strain amplitude versus frequency (Pipkin diagram). The biofilms also exhibit variability in the onset of nonlinear behaviour and energy dissipation characteristics, which could be a result of heterogeneity of the extracellular matrix constituents of the different biofilms. The results provide insight into the nonlinear rheological behaviour of biofilms as they are subjected to large strains or strain rates; a situation that is commonly encountered in nature, but rarely investigated.

Highlights

Bacterial biofilms occur in diverse environments, such as aquifers[1], rivers[2,3], hydrothermal springs[4], within sewer pipelines[5], in bioremediation plants[6] and various other places
The ability of biofilms to withstand the above-mentioned dynamic environments is often attributed to the extracellular matrix (ECM),[12,13] which is commonly described as a network of polymers, including extracellular polysaccharides (EPS), extracellular DNA, proteins and various other components[14]
The biofilms exhibit differences in transition to nonlinear viscoelastic behaviour and energy dissipation characteristics, indicating that polymeric composition can play a role in dictating such nonlinear behaviours. These results show that Large Amplitude Oscillatory Shear (LAOS) can be a useful tool in characterising the nonlinear rheological behaviour in biofilms of different species

Summary

Introduction

Bacterial biofilms occur in diverse environments, such as aquifers[1], rivers[2,3], hydrothermal springs[4], within sewer pipelines[5], in bioremediation plants[6] and various other places Within these environments the biofilms can be subjected to extreme temperatures[4,7], variation in physical forces[8], changes in chemical concentrations[9], changes in salinity[10] and pH11. Since the polymeric composition and its organisation within the ECM dictates the rheological behaviour of the biofilms (in addition to other functionalities); it becomes important to investigate the matrix viscoelasticity[17,18,19]. This could allow one to understand the role of biopolymers in conferring structure to the biofilm, and, its biological and environmental functionalities

Objectives

Methods

Results