The role of biofilm matrix composition in controlling colony expansion and morphology

Abstract

Biofilms are biological viscoelastic gels composed of bacterial cells embedded in a self-secreted polymeric extracellular matrix (ECM). In environmental settings, such as in the rhizosphere and phyllosphere, biofilm colonization occurs at the solid–air interface. The biofilms’ ability to colonize and expand over these surfaces depends on the formation of osmotic gradients and ECM viscoelastic properties. In this work, we study the influence of biofilm ECM components on its viscoelasticity and expansion, using the model organism Bacillus subtilis and deletion mutants of its three major ECM components, TasA, EPS and BslA. Using a multi-scale approach, we quantified macro-scale viscoelasticity and expansion dynamics. Furthermore, we used a microsphere assay to visualize the micro-scale expansion patterns. We find that the viscoelastic phase angle Φ is likely the best viscoelastic parameter correlating to biofilm expansion dynamics. Moreover, we quantify the sensitivity of the biofilm to changes in substrate water potential as a function of ECM composition. Finally, we find that the deletion of ECM components significantly increases the coherence of micro-scale colony expansion patterns. These results demonstrate the influence of ECM viscoelasticity and substrate water potential on the expansion of biofilm colonies on wet surfaces at the air–solid interface, commonly found in natural environments.

Extracellular proteases are an essential public good supportingBacillus subtilisgrowth through exogenous protein degradation

“…B. subtilis produces many public goods including specialised metabolites with antimicrobial activity (42) and structural components of the biofilm extracellular matrix (43)(44)(45). The cost incurred by the cells when producing public goods is variable and can be context-dependent (46)(47)(48).…”

Editorial: theme issue on complex rheology in biological systems

“…For this theme issue, we gratefully received contributions from across the physics and life sciences with interests in biorheology ranging in length scale from the rheological properties of intracellular biomolecular networks [ 1 , 10 ] to the scale of the direct extracellular environment [ 3 , 7 , 10 , 12 , 13 , 16 ], tissues [ 3 – 5 ] and even entire organs that actively exert forces onto non-Newtonian fluids [ 6 ]. The mechanical properties at the cellular level are discussed in relationship to cancer [ 2 ], as well as in relationship to the transport of red blood cells in disordered porous environments, be it in vascular networks or in microfluidic devices.…”

“…The mechanical properties at the cellular level are discussed in relationship to cancer [ 2 ], as well as in relationship to the transport of red blood cells in disordered porous environments, be it in vascular networks or in microfluidic devices. The interaction of a cell with its environment, and in particular the consequence of these interactions to cell mobility, is discussed in the context of (i) blood flow in vascular networks [ 5 ], (ii) male infertility [ 7 ], (iii) the stability of biofilms [ 12 , 13 ] and (iv) new opportunities of using liquid crystals to impose controlled constraints to cell motion [ 16 ].…”

“…haematology) is clearly a field where rheology is vital [ 5 ], but other key rheological control problems emerge in digestive [ 6 ] and reproductive biology [ 7 ]. Other biological flows contain rheologically induced structural or phase transitions, and the understanding of how biological fluids and soft solids flow and deform is a key scientific area within this collaboration of physical and life sciences (blood [ 8 ], the cytosol, silk protein solutions [ 9 ], saliva, mucus [ 10 ], synovial fluid, biofilms [ 11 – 13 ], tissue buckling [ 14 ], bacterial rheotaxis [ 15 ] and E. coli bacteria swimming in media with liquid crystalline order [ 16 ] are just some examples [ 17 ]).…”

Microstructural and Rheological Transitions in Bacterial Biofilms

“…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.…”