Energetics of mesoscale cell turbulence in two-dimensional monolayers

Shao-Zhen Lin,Wu-Yang Zhang,Xi-Qiao Feng,Dapeng Bi,Bo Li

doi:10.1038/s42005-021-00530-6

Shao-Zhen Lin, Wu-Yang Zhang + Show 3 more

Open Access

https://doi.org/10.1038/s42005-021-00530-6

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Abstract

Investigation of energy mechanisms at the collective cell scale is a challenge for understanding various biological processes, such as embryonic development and tumor metastasis. Here we investigate the energetics of self-sustained mesoscale turbulence in confluent two-dimensional (2D) cell monolayers. We find that the kinetic energy and enstrophy of collective cell flows in both epithelial and non-epithelial cell monolayers collapse to a family of probability density functions, which follow the q-Gaussian distribution rather than the Maxwell–Boltzmann distribution. The enstrophy scales linearly with the kinetic energy as the monolayer matures. The energy spectra exhibit a power-decaying law at large wavenumbers, with a scaling exponent markedly different from that in the classical 2D Kolmogorov–Kraichnan turbulence. These energetic features are demonstrated to be common for all cell types on various substrates with a wide range of stiffness. This study provides unique clues to understand active natures of cell population and tissues.

Highlights

Investigation of energy mechanisms at the collective cell scale is a challenge for understanding various biological processes, such as embryonic development and tumor metastasis
The field of view (FOV) has size 1.33 mm × 1.33 mm, which is much larger than the spatial correlation length (~200–300 μm) of mesoscale cell turbulence[16,18,19], and large enough to access its energetic statistics
Using living cell imaging on confluent cell monolayer systems consisting of different cell types and various substrates, we probe the energetics of mesoscale cell turbulence emerging in 2D cell sheets

Summary

Introduction

Investigation of energy mechanisms at the collective cell scale is a challenge for understanding various biological processes, such as embryonic development and tumor metastasis. The energy spectra exhibit a power-decaying law at large wavenumbers, with a scaling exponent markedly different from that in the classical 2D Kolmogorov–Kraichnan turbulence. These energetic features are demonstrated to be common for all cell types on various substrates with a wide range of stiffness. The enstrophy scales proportionally to the kinetic energy, which generalizes previous findings[23,28] to monolayers of diverse cell lines, suggesting a common feature in living multicellular systems. The energy spectra of mesoscale cell turbulence are profoundly different from that in the classical 2D Kolmogorov–Kraichnan turbulence These features are common across different cell types, and insensitive to the substrate stiffness. An active vertex model is used to reveal the physical mechanisms underlying these energetic statistics

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