Self-regulation of phenotypic noise synchronizes emergent organization and active transport in confluent microbial environments

in Nature Physics (2022)

The variation associated with different observable characteristics—phenotypes—at the cellular scale underpins homeostasis and the fitness of living systems. However, if and how these noisy phenotypic ... [more ▼]

The variation associated with different observable characteristics—phenotypes—at the cellular scale underpins homeostasis and the fitness of living systems. However, if and how these noisy phenotypic traits shape properties at the population level remains poorly understood. Here we report that phenotypic noise self-regulates with growth and coordinates collective structural organization, the kinetics of topological defects and the emergence of active transport around confluent colonies. We do this by cataloguing key phenotypic traits in bacteria growing under diverse conditions. Our results reveal a statistically precise critical time for the transition from a monolayer biofilm to a multilayer biofilm, despite the strong noise in the cell geometry and the colony area at the onset of the transition. This reveals a mitigation mechanism between the noise in the cell geometry and the growth rate that dictates the narrow critical time window. By uncovering how rectification of phenotypic noise homogenizes correlated collective properties across colonies, our work points at an emergent strategy that confluent systems employ to tune active transport, buffering inherent heterogeneities associated with natural cellular environment settings. [less ▲]

Mono-to-multilayer transition in growing bacterial colonies

in Physical Review Letters (2019), 123(17-25),

The transition from monolayers to multilayered structures in bacterial colonies is a fundamental step in biofilm development. Observed across different morphotypes and species, this transition is ... [more ▼]

The transition from monolayers to multilayered structures in bacterial colonies is a fundamental step in biofilm development. Observed across different morphotypes and species, this transition is triggered within freely growing bacterial microcolonies comprising a few hundred cells. Using a combination of numerical simulations and analytical modeling, here we demonstrate that this transition originates from the competition between growth-induced in-plane active stresses and vertical restoring forces, due to the cell-substrate interactions. Using a simple chainlike colony of laterally confined cells, we show that the transition sets when individual cells become unstable to rotations; thus it is localized and mechanically deterministic. Asynchronous cell division renders the process stochastic, so that all the critical parameters that control the onset of the transition are continuously distributed random variables. Here we demonstrate that the occurrence of the first division in the colony can be approximated as a Poisson process in the limit of large cell numbers. This allows us to approximately calculate the probability distribution function of the position and time associated with the first extrusion. The rate of such a Poisson process can be identified as the order parameter of the transition, thus highlighting its mixed deterministic-stochastic nature. [less ▲]