A mechanistic understanding of biofilm morphogenesis: Coexistence of mobile and sessile aggregates and phase-separated patterns

Most bacteria in the natural environment self-organize into collective phases such as cell clusters, swarms, patterned colonies, or biofilms. The occurrence of different phases and their coexistence is governed by several intrinsic and extrinsic factors such as the growth, motion, and physicochemical interactions. Hence, it is crucial to predict the conditions under which a collective phase emerges due to the individual-level interactions. Here we develop a particle-based biophyiscal model of bacterial cells and self-secreted extracellular polymeric substances (EPS) to decipher the interplay of growth, motility-mediated dispersal, and mechanical interactions during microcolony morphogenesis. We show that depending upon the heterogeneous production and physicochemical properties of EPS, whether sticky or nonadsorbing in nature, the microcolony dynamics and architecture significantly varies. In particular, in sticky EPS, microcolony shows the coexistence of both motile and sessile aggregates rendering a transition towards biofilm formation. Wherein for the nonad-sorbing EPS, which behaves as depletant in the media, a variety of phase-segregated patterned colonies either localizing the matrix component or cells at the colony periphery may emerge. We identified that the interplay of differential dispersion and the mechanical interactions among the components of the colony determines the fate of the colony morphology. Our results provide a significant understanding of the mechano-self-regulation during biofilm morphogenesis and open up possibilities of designing experiments to test the predictions.