Biofilm self-patterning: mechanical forces drive a reorientation cascade

TL;DR

This study uncovers how mechanical forces and cell growth dynamics drive a self-organized, long-range patterning in Vibrio cholerae biofilms, revealing a cascade of cell reorientations that shape biofilm structure.

Contribution

It demonstrates the role of mechanical forces in biofilm pattern formation and introduces a combined experimental and modeling approach to understand this process.

Findings

Cell verticalization in the core induces differential growth.

Radial rim alignment generates compressive stresses.

Self-patterning is dependent on cell-surface adhesion.

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, which are surface-attached aggregates of bacterial cells embedded in an extracellular matrix. However, how bacterial growth coordinates with cell-surface interactions to create distinctive, long-range order in biofilms remains elusive. Here we report a collective cell reorientation cascade in growing Vibrio cholerae biofilms, leading to a differentially ordered, spatiotemporally coupled core-rim structure reminiscent of a blooming aster. Cell verticalization in the core generates differential growth that drives radial alignment of the cells in the rim, while the radially aligned rim in turn generates compressive stresses that expand the verticalized core. Such self-patterning disappears in adhesion-less mutants but can be restored through opto-manipulation of growth. Agent-based simulations and two-phase active nematic modeling reveal the strong interdependence of the driving forces for the differential ordering. Our findings provide insight into the collective cell patterning in bacterial communities and engineering of phenotypes and functions of living active matter.