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Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system

Trichoplax adhaerens is a small, ciliated marine animal that glides on surfaces grazing upon algae, which it digests externally. It has no muscles or nervous system and only six cell types, all but two of which are embedded in its epithelium. The epithelial cells are joined by apical adherens juncti...

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Autores principales: Smith, Carolyn L., Reese, Thomas S., Govezensky, Tzipe, Barrio, Rafael A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6500112/
https://www.ncbi.nlm.nih.gov/pubmed/30979806
http://dx.doi.org/10.1073/pnas.1815655116
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author Smith, Carolyn L.
Reese, Thomas S.
Govezensky, Tzipe
Barrio, Rafael A.
author_facet Smith, Carolyn L.
Reese, Thomas S.
Govezensky, Tzipe
Barrio, Rafael A.
author_sort Smith, Carolyn L.
collection PubMed
description Trichoplax adhaerens is a small, ciliated marine animal that glides on surfaces grazing upon algae, which it digests externally. It has no muscles or nervous system and only six cell types, all but two of which are embedded in its epithelium. The epithelial cells are joined by apical adherens junctions; neither tight junctions nor gap junctions are present. Monociliated epithelial cells on the lower surface propel gliding. The cilia beat regularly, but asynchronously, and transiently contact the substrate with each stroke. The animal moves in random directions in the absence of food. We show here that it exhibits chemotaxis, moving preferentially toward algae embedded in a disk of agar. We present a mathematical model to explain how coherent, directional movements could arise from the collective actions of a set of ciliated epithelial cells, each independently sensing and responding to a chemoattractant gradient. The model incorporates realistic values for viscoelastic properties of cells and produces coordinated movements and changes in body shape that resemble the actual movements of the animal. The model demonstrates that an animal can move coherently in search of food without any need for chemical signaling between cells and introduces a different approach to modeling behavior in primitive multicellular organisms.
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spelling pubmed-65001122019-05-20 Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system Smith, Carolyn L. Reese, Thomas S. Govezensky, Tzipe Barrio, Rafael A. Proc Natl Acad Sci U S A PNAS Plus Trichoplax adhaerens is a small, ciliated marine animal that glides on surfaces grazing upon algae, which it digests externally. It has no muscles or nervous system and only six cell types, all but two of which are embedded in its epithelium. The epithelial cells are joined by apical adherens junctions; neither tight junctions nor gap junctions are present. Monociliated epithelial cells on the lower surface propel gliding. The cilia beat regularly, but asynchronously, and transiently contact the substrate with each stroke. The animal moves in random directions in the absence of food. We show here that it exhibits chemotaxis, moving preferentially toward algae embedded in a disk of agar. We present a mathematical model to explain how coherent, directional movements could arise from the collective actions of a set of ciliated epithelial cells, each independently sensing and responding to a chemoattractant gradient. The model incorporates realistic values for viscoelastic properties of cells and produces coordinated movements and changes in body shape that resemble the actual movements of the animal. The model demonstrates that an animal can move coherently in search of food without any need for chemical signaling between cells and introduces a different approach to modeling behavior in primitive multicellular organisms. National Academy of Sciences 2019-04-30 2019-04-12 /pmc/articles/PMC6500112/ /pubmed/30979806 http://dx.doi.org/10.1073/pnas.1815655116 Text en Copyright © 2019 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle PNAS Plus
Smith, Carolyn L.
Reese, Thomas S.
Govezensky, Tzipe
Barrio, Rafael A.
Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system
title Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system
title_full Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system
title_fullStr Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system
title_full_unstemmed Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system
title_short Coherent directed movement toward food modeled in Trichoplax, a ciliated animal lacking a nervous system
title_sort coherent directed movement toward food modeled in trichoplax, a ciliated animal lacking a nervous system
topic PNAS Plus
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6500112/
https://www.ncbi.nlm.nih.gov/pubmed/30979806
http://dx.doi.org/10.1073/pnas.1815655116
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