Modelling multiscale architecture of biofilm extracellular matrix and its role in oxygen transport

Abstract

The extracellular matrix of biofilms presents a dense and intricate architecture. Numerous biophysical properties of the matrix surrounding microbial cells contribute to the heterogeneity of biofilms and their functions at the microscale. Previous mathematical models assume the matrix to be homogeneous, often overlooking the need for a detailed mechanistic understanding of the extracellular space. In this theoretical study, we introduce a novel cell-capsule approach to investigate geometric patterns in biofilm morphology and predict their role in oxygen transport. The thickness of the capsule and the arrangement of cell-capsule patterns can influence matrix heterogeneity, providing a clear picture of biofilm structure. By incorporating the bacterial capsule as a distinct, low-diffusivity phase, our novel cell-capsule model reveals that this architecture acts as a significant 'resistance-in-series' barrier. We found that a thick capsule/dense matrix arrangement can reduce local oxygen transfer by approximately 70%, a substantial drop that may give drive further research into oxygen limitations during early stage biofilm development.