The Interplay of Adhesion, Friction, and Nutrient Availability in Modulating Biofilm Wrinkling Behavior

Wrinkled patterns in bacterial biofilms regulate the transport of nutrients, oxygen, and microorganisms, impacting their capacity to adapt to environmental stress. Nutrient availability, friction, and adhesion are known to influence biofilm wrinkling, but their interplay and the role of heterogeneity in adhesion, remain poorly understood. Here, we introduce a novel lattice-network model of biofilm morphogenesis to address that gap. Under uniform nutrient supply, increasing friction accelerates stress buildup, causing wrinkling at smaller radii and higher critical stresses. In contrast, increasing adhesion raises the critical stress but delays wrinkling to larger radii—contradicting classical buckling theory and suggesting a decoupling between the overall biofilm size and the length scale governing the instability. Introducing adhesion heterogeneity lowers the critical buckling stress by promoting wrinkle formation in weakly adhered regions, though the magnitude of this effect depends strongly on both average adhesion and friction. Notably, nutrient availability controls the wrinkling evolution. For uniform nutrients, the wrinkling mechanism remains consistent despite variations of more than two orders of magnitude in both friction and adhesion. Under nonuniform nutrient conditions, we identify and confirm experimentally in E. coli, a previously unreported transition in the wrinkling evolution mechanism. With abundant nutrients, growth remains spatially uniform, and wrinkles initiate at the center and propagate outward. At low nutrient levels, early nutrient depletion halts growth in the center, causing wrinkles to first appear at the nutrient-rich edge and propagate inward. Our work offers mechanistic understanding for how natural biofilms may exploit physical interactions like friction or adhesion to modulate their wrinkling response.