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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Format: | Article |
Language: | English |
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IOP Publishing
2022-01-01
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Series: | New Journal of Physics |
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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. |
first_indexed | 2024-03-12T16:04:37Z |
format | Article |
id | doaj.art-75916112300043c1bb6794dc79264016 |
institution | Directory Open Access Journal |
issn | 1367-2630 |
language | English |
last_indexed | 2024-03-12T16:04:37Z |
publishDate | 2022-01-01 |
publisher | IOP Publishing |
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series | New Journal of Physics |
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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