Mechanical forces drive a reorientation cascade leading to biofilm self-patterning

Abstract

In growing active matter systems, a large collection of engineered or living autonomous units metabolize free energy and create order at different length scales as they proliferate and migrate collectively. One such example is bacterial biofilms, surface-attached aggregates of bacterial cells embedded in an extracellular matrix that can exhibit community-scale orientational order. However, how bacterial growth coordinates with cell-surface interactions to create distinctive, long-range order during biofilm development remains elusive. Here we report a collective cell reorientation cascade in growing Vibrio cholerae biofilms that leads to a differentially ordered, spatiotemporally coupled core-rim structure reminiscent of a blooming aster. Cell verticalization in the core leads to a pattern of differential growth that drives radial alignment of the cells in the rim, while the growing rim generates compressive stresses that expand the verticalized core. Such self-patterning disappears in nonadherent mutants but can be restored through opto-manipulation of growth. Agent-based simulations and two-phase active nematic modeling jointly reveal the strong interdependence of the driving forces underlying the differential ordering. Our findings offer insight into the developmental processes that shape bacterial communities and provide ways to engineer phenotypes and functions in living active matter.