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

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...

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Main Authors: Yoav G Pollack, Philip Bittihn, Ramin Golestanian
Format: Article
Language:English
Published: IOP Publishing 2022-01-01
Series:New Journal of Physics
Subjects:
Online Access:https://doi.org/10.1088/1367-2630/ac788e
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author Yoav G Pollack
Philip Bittihn
Ramin Golestanian
author_facet Yoav G Pollack
Philip Bittihn
Ramin Golestanian
author_sort Yoav G Pollack
collection DOAJ
description 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 for this specific kind of 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.
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spelling doaj.art-75916112300043c1bb6794dc792640162023-08-09T14:24:57ZengIOP PublishingNew Journal of Physics1367-26302022-01-0124707300310.1088/1367-2630/ac788eA competitive advantage through fast dead matter elimination in confined cellular aggregatesYoav G Pollack0https://orcid.org/0000-0002-9703-6127Philip Bittihn1https://orcid.org/0000-0002-1276-9381Ramin Golestanian2https://orcid.org/0000-0002-3149-4002Max Planck Institute for Dynamics and Self-Organization (MPIDS) , 37077 Göttingen, GermanyMax Planck Institute for Dynamics and Self-Organization (MPIDS) , 37077 Göttingen, GermanyMax Planck Institute for Dynamics and Self-Organization (MPIDS) , 37077 Göttingen, Germany; Rudolf Peierls Centre for Theoretical Physics, University of Oxford , Oxford OX1 3PU, United KingdomCompetition 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 for this specific kind of 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.https://doi.org/10.1088/1367-2630/ac788ecellstissue homeostasiscompetitionmechanical pressuregrowing active matterpassive matter
spellingShingle Yoav G Pollack
Philip Bittihn
Ramin Golestanian
A competitive advantage through fast dead matter elimination in confined cellular aggregates
New Journal of Physics
cells
tissue homeostasis
competition
mechanical pressure
growing active matter
passive matter
title A competitive advantage through fast dead matter elimination in confined cellular aggregates
title_full A competitive advantage through fast dead matter elimination in confined cellular aggregates
title_fullStr A competitive advantage through fast dead matter elimination in confined cellular aggregates
title_full_unstemmed A competitive advantage through fast dead matter elimination in confined cellular aggregates
title_short A competitive advantage through fast dead matter elimination in confined cellular aggregates
title_sort competitive advantage through fast dead matter elimination in confined cellular aggregates
topic cells
tissue homeostasis
competition
mechanical pressure
growing active matter
passive matter
url https://doi.org/10.1088/1367-2630/ac788e
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