Colony morphogenesis regulates sporulation dynamics in bacterial biofilms

Abstract

In multicellular systems, organized phenotypic heterogeneity emerges from the interplay of processes spanning scales from molecular to population-level. Using Bacillus subtilis, we investigated feedback between the collective process of colony expansion and the distribution of spore development among individual cells, a process triggered by starvation. Biofilms are commonly studied using a strain with inhibited sporulation. Intact regulation yielded high-frequency sporulation early in biofilm growth. Biofilm composition was organized by a wave of sporulation driving biofilms toward dormancy from within. However, expansion was also maintained by non-sporulating cells in a narrow front at the external edge. Along with mathematical modeling, we also used mutants with altered biofilm morphogenesis to probe the relationship between colony expansion and sporulation. Sporulation dynamics were patterned by radial expansion, but the faster biofilms spread, the greater the separation of growth and sporulation distributions. We demonstrate essential interplay between cell behavior and the physics of collective expansion that organizes differentiation among cells.