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

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.

Roughening instability of growing 3D bacterial colonies

“…Indeed, similar 3D patterns of rough growth have been observed in other living systems, namely in multicellular clusters of Saccharomyces cerevisiae, usually referred to as 'snowflake yeast clusters', or in aggregation clusters of the green alga Volvox carteri. Recent research has shown that the sizes and morphologies of these clusters are crucially determined by growth and crowdinginduced mechanical stresses coupled to environment conditions [143][144][145][146][147]. These works have suggested the tantalizing idea that the morphological adaptation of large 3D clusters to environmental constraints could provide insight into the origins of multicellularity.…”

Varied solutions to multicellularity: The biophysical and evolutionary consequences of diverse intercellular bonds

“…However, the inherent stochasticity of the cell division process, combined with any curvature of the tissue, makes it unlikely that crystalline arrangements of cells will prevail across the entire organism. 18 In experimental images of select cases, we indeed see that the intercellular bond network has a disorder (see, e.g., Refs. 18 and 73 and Fig.…”

“… 18 In experimental images of select cases, we indeed see that the intercellular bond network has a disorder (see, e.g., Refs. 18 and 73 and Fig. 3 ).…”

“…3 ), the observed distribution of volume per cell was found to match the predicted distribution from maximum entropy considerations. 18 Their cellular spatial structure was remarkably reproducible, even without explicit developmental patterning, underpinning the emergence of novel, heritable multicellular traits that arise from the mechanics of cellular packing. 18,76 Entropic effects on cell packing are not only simply a factor for small, undifferentiated groups of cells but have also been observed to affect organisms that possess complex developmental regulation.…”

“… 16,17 How does the attachment mechanism impact the geometry of cell arrangements? 18 How likely are physical forces to fragment entire organisms into separate pieces? 16,19 How do tissue-level mechanical properties emerge from cellular properties and behavior?…”