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

Day, Thomas C; Höhn, Stephanie S; Zamani-Dahaj, Seyed A; Yanni, David; Burnetti, Anthony; Pentz, Jennifer; Honerkamp-Smith, Aurelia R; Wioland, Hugo et al. · Elife · 2022

basic_science · Level V

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Abstract

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 <i>Volvox carteri</i>. 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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