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Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor

Evolution of multicellularity from early unicellular ancestors is arguably one of the most important transitions since the origin of life(1,2). Multicellularity is often associated with higher nutrient uptake(3), better defense against predation, cell specialization and better division of labor(4)....

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Autores principales: Shekhar, Shashank, Guo, Hanliang, Colin, Sean P., Marshall, Wallace, Kanso, Eva, Costello, John H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9882025/
https://www.ncbi.nlm.nih.gov/pubmed/36711609
http://dx.doi.org/10.1101/2023.01.10.523506
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author Shekhar, Shashank
Guo, Hanliang
Colin, Sean P.
Marshall, Wallace
Kanso, Eva
Costello, John H.
author_facet Shekhar, Shashank
Guo, Hanliang
Colin, Sean P.
Marshall, Wallace
Kanso, Eva
Costello, John H.
author_sort Shekhar, Shashank
collection PubMed
description Evolution of multicellularity from early unicellular ancestors is arguably one of the most important transitions since the origin of life(1,2). Multicellularity is often associated with higher nutrient uptake(3), better defense against predation, cell specialization and better division of labor(4). While many single-celled organisms exhibit both solitary and colonial existence(3,5,6), the organizing principles governing the transition and the benefits endowed are less clear. Using the suspension-feeding unicellular protist Stentor coeruleus, we show that hydrodynamic coupling between proximal neighbors results in faster feeding flows that depend on the separation between individuals. Moreover, we find that the accrued benefits in feeding current enhancement are typically asymmetric– individuals with slower solitary currents gain more from partnering than those with faster currents. We find that colony-formation is ephemeral in Stentor and individuals in colonies are highly dynamic unlike other colony-forming organisms like Volvox carteri (3). Our results demonstrate benefits endowed by the colonial organization in a simple unicellular organism and can potentially provide fundamental insights into the selective forces favoring early evolution of multicellular organization.
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spelling pubmed-98820252023-01-28 Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor Shekhar, Shashank Guo, Hanliang Colin, Sean P. Marshall, Wallace Kanso, Eva Costello, John H. bioRxiv Article Evolution of multicellularity from early unicellular ancestors is arguably one of the most important transitions since the origin of life(1,2). Multicellularity is often associated with higher nutrient uptake(3), better defense against predation, cell specialization and better division of labor(4). While many single-celled organisms exhibit both solitary and colonial existence(3,5,6), the organizing principles governing the transition and the benefits endowed are less clear. Using the suspension-feeding unicellular protist Stentor coeruleus, we show that hydrodynamic coupling between proximal neighbors results in faster feeding flows that depend on the separation between individuals. Moreover, we find that the accrued benefits in feeding current enhancement are typically asymmetric– individuals with slower solitary currents gain more from partnering than those with faster currents. We find that colony-formation is ephemeral in Stentor and individuals in colonies are highly dynamic unlike other colony-forming organisms like Volvox carteri (3). Our results demonstrate benefits endowed by the colonial organization in a simple unicellular organism and can potentially provide fundamental insights into the selective forces favoring early evolution of multicellular organization. Cold Spring Harbor Laboratory 2023-01-12 /pmc/articles/PMC9882025/ /pubmed/36711609 http://dx.doi.org/10.1101/2023.01.10.523506 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Shekhar, Shashank
Guo, Hanliang
Colin, Sean P.
Marshall, Wallace
Kanso, Eva
Costello, John H.
Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor
title Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor
title_full Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor
title_fullStr Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor
title_full_unstemmed Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor
title_short Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor
title_sort cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate stentor
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9882025/
https://www.ncbi.nlm.nih.gov/pubmed/36711609
http://dx.doi.org/10.1101/2023.01.10.523506
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