4.8 Article

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

Journal

NATURE PHYSICS
Volume 18, Issue 8, Pages 945-+

Publisher

NATURE PORTFOLIO
DOI: 10.1038/s41567-022-01641-9

Keywords

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Funding

  1. Luxembourg National Research Fund, under the PRIDE Doctoral Training Unit [MICROH: PRIDE17/11823097]
  2. AFR-Grant [13563560]
  3. ATTRACT Investigator Grant [A17/MS/11572821/MBRACE]
  4. Human Frontier Science Program Cross Disciplinary Fellowship [LT000368/2019-C]
  5. ERC-CoG grant HexaTissue
  6. Netherlands Organization for Scientific Research (NWO/OCW)

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This study explores the self-regulation of phenotypic noise and its coordination with collective structural organization, topological defects kinetics, and active transport emergence in bacterial colonies. Despite noise in cell geometry and colony area, there is a statistically precise critical time for the transition from a monolayer biofilm to a multilayer biofilm. By rectifying phenotypic noise, the study reveals an emergent strategy of confluent systems to tune active transport and buffer inherent heterogeneities.
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. The first step of biofilm formation is a transition from a single layer of bacteria to multiple layers. Now, there is evidence that this transition is determined by the phenotypic noise associated with cell geometry and growth rate.

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