Mechanical constraints to unbound expansion of B. subtilis on semi-solid surfaces

Abstract

ABSTRACT The effects of surface mechanical constraints that may promote or prevent bacterial expansion on semi-solid surfaces are largely unknown. In this work, we have manufactured agar surfaces with different viscoelasticity, topography, and roughness. To capture the essential biophysics of the bacterial expansion we have developed a continuum model that faithfully reproduces the main patterns of the short-range and long-range expansion with two critical parameters: local interfacial forces and colony viscosity. Cohesive energy of the bacterial colony that determines the extent of exploration was dependent on agar surface viscoelasticity. On soft surfaces, bacteria produce low viscoelastic colonies that allow guided population of bacteria to traverse distances that are six orders of magnitude larger than the size of the individual bacterium. Bacteria growing on stiff surfaces produce colonies with significantly increased viscoelasticity that prevent bacterial exploration of new territory and allow formation of a very steep cliff at the edge of the colony. Upon flooding of the rough surfaces, we have induced aquaplaning and spreading of bacteria. A layer of water between the bacterium and surface results in a loss of traction allowing bacteria to spread across the otherwise inhibitory rough surface. The results shed new light on the bacterial ability to rapidly colonize new territories. IMPORTANCE How bacterial cells colonize new territory is a problem of fundamental microbiological and biophysical interest and is key to the emergence of several phenomena of biological, ecological, and medical relevance. Here, we demonstrate how bacteria stuck in a colony of finite size can resume exploration of new territory by aquaplaning and how they fine tune biofilm viscoelasticity to surface material properties that allows them differential mobility. We show how changing local interfacial forces and colony viscosity results in a plethora of bacterial morphologies on surfaces with different physical and mechanical properties.