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A competitive advantage through fast dead matter elimination in confined cellular aggregates

Yoav G. Pollack, View ORCID ProfilePhilip Bittihn, View ORCID ProfileRamin Golestanian
doi: https://doi.org/10.1101/2021.07.22.453340
Yoav G. Pollack
1Max Planck Institute for Dynamics and Self-Organization (MPIDS), 37077 Göttingen, Germany
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Philip Bittihn
1Max Planck Institute for Dynamics and Self-Organization (MPIDS), 37077 Göttingen, Germany
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Ramin Golestanian
1Max Planck Institute for Dynamics and Self-Organization (MPIDS), 37077 Göttingen, Germany
2Rudolf Peierls Centre for Theoretical Physics, University of Oxford, Oxford, OX1 3PU, UK
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  • For correspondence: ramin.golestanian@ds.mpg.de
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Abstract

Competition of different species or cell types for limited space is relevant in a variety of biological processes such as biofilm development, tissue morphogenesis and tumor growth. Predicting the outcome for non-adversarial competition of such growing active matter is non-trivial, as it depends on how processes like growth, proliferation and the degradation of cellular matter are regulated in confinement; regulation that happens even in the absence of competition to achieve the dynamic steady state known as homeostasis. Here, we show that passive by-products of the processes maintaining homeostasis can significantly alter fitness. Even for purely pressure-regulated growth and exclusively mechanical interactions, this enables cell types with lower homeostatic pressure to outcompete those with higher homeostatic pressure. We reveal that interfaces play a critical role in the competition: There, growing matter with a higher proportion of active cells can better exploit local growth opportunities that continuously arise as the active processes keep the system out of mechanical equilibrium. We elucidate this effect in a theoretical toy model and test it in an agent-based computational model that includes finite-time mechanical persistence of dead cells and thereby decouples the density of growing cells from the homeostatic pressure. Our results suggest that self-organization of cellular aggregates into active and passive matter can be decisive for competition outcomes and that optimizing the proportion of growing (active) cells can be as important to survival as sensitivity to mechanical cues.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 23, 2021.
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A competitive advantage through fast dead matter elimination in confined cellular aggregates
Yoav G. Pollack, Philip Bittihn, Ramin Golestanian
bioRxiv 2021.07.22.453340; doi: https://doi.org/10.1101/2021.07.22.453340
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A competitive advantage through fast dead matter elimination in confined cellular aggregates
Yoav G. Pollack, Philip Bittihn, Ramin Golestanian
bioRxiv 2021.07.22.453340; doi: https://doi.org/10.1101/2021.07.22.453340

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