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

Thomas C. Day; Stephanie S. Hohn; 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

arXiv · 2108.00425

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

Thomas C. Day·Stephanie S. Hohn·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

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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 $Volvox~carteri$. 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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Thomas C. Day, Stephanie S. Hohn, 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. 2021-08-01. Cellular organization in lab-evolved and extant multicellular species obeys a maximum entropy law. https://arxiv.org/abs/2108.00425

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