eLife (Feb 2022)

Cellular organization in lab-evolved and extant multicellular species obeys a maximum entropy law

  • Thomas C Day,
  • Stephanie S Höhn,
  • Seyed A Zamani-Dahaj,
  • David Yanni,
  • Anthony Burnetti,
  • Jennifer Pentz,
  • Aurelia R Honerkamp-Smith,
  • Hugo Wioland,
  • Hannah R Sleath,
  • William C Ratcliff,
  • Raymond E Goldstein,
  • Peter J Yunker

DOI
https://doi.org/10.7554/eLife.72707
Journal volume & issue
Vol. 11

Abstract

Read online

The prevalence of multicellular organisms is due in part to their ability to form complex structures. How cells pack in these structures is a fundamental biophysical issue, underlying their functional properties. However, much remains unknown about how cell packing geometries arise, and how they are affected by random noise during growth - especially absent developmental programs. Here, we quantify the statistics of cellular neighborhoods of two different multicellular eukaryotes: lab-evolved ‘snowflake’ yeast and the green alga Volvox carteri. We find that despite large differences in cellular organization, the free space associated with individual cells in both organisms closely fits a modified gamma distribution, consistent with maximum entropy predictions originally developed for granular materials. This ‘entropic’ cellular packing ensures a degree of predictability despite noise, facilitating parent-offspring fidelity even in the absence of developmental regulation. Together with simulations of diverse growth morphologies, these results suggest that gamma-distributed cell neighborhood sizes are a general feature of multicellularity, arising from conserved statistics of cellular packing.

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