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

Author:

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

Abstract

AbstractThe 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.

Publisher

Cold Spring Harbor Laboratory

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