A multiscale study of bacterial biofilms. From isolated components to multicellular organisms

Abstract

Biofilms are multicellular microbial communities that encase themselves in a secreted network of biopolymers and attach to surfaces and interfaces. From a soft matter perspective, biofilms are regarded as colloidal hydrogels, with the cells playing the role of colloids and the extracellular matrix (ECM) compared with a cross-linked hydrogel. However, from a biological perspective, biofilms are heterogeneous communities that organize in space and time into functionally distinct subgroups, in a process resembling differentiation in higher organisms. Biofilm heterogeneity has been demonstrated at the cellular level, but the molecular level has been neglected. In this talk I discuss the soft matter and biological perspectives of biofilms, focusing on the properties of water, ECM, and metal ions. Using simultaneous X-ray diffraction/fluorescence (XRD/XRF), we portrayed the dominant structural features in Bacillus subtilis biofilms and mapped them in space and time. Particularly, we revealed molecular-level structural hierarchy in the biofilms, that followed biofilm macroscopic morphology. Mapping the XRD and XRF signatures of intact biofilms in space and time allowed us to suggest an inclusive view of biofilm development, linking the ECM and the spores via the transport of water and metal ions. Our findings demonstrate that biofilm heterogeneity is not only affected by local genetic expression and cellular differentiation but also by passive effects resulting from the physicochemical properties of the molecules secreted by the cells. This study unravels the importance of molecular-level heterogeneity in shaping biofilm physiology and development.