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A mechanistic explanation of the transition to simple multicellularity in fungi

Development of multicellularity was one of the major transitions in evolution and occurred independently multiple times in algae, plants, animals, and fungi. However recent comparative genome analyses suggest that fungi followed a different route to other eukaryotic lineages. To understand the drivi...

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Autores principales: Heaton, Luke L. M., Jones, Nick S., Fricker, Mark D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7244713/
https://www.ncbi.nlm.nih.gov/pubmed/32444651
http://dx.doi.org/10.1038/s41467-020-16072-4
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author Heaton, Luke L. M.
Jones, Nick S.
Fricker, Mark D.
author_facet Heaton, Luke L. M.
Jones, Nick S.
Fricker, Mark D.
author_sort Heaton, Luke L. M.
collection PubMed
description Development of multicellularity was one of the major transitions in evolution and occurred independently multiple times in algae, plants, animals, and fungi. However recent comparative genome analyses suggest that fungi followed a different route to other eukaryotic lineages. To understand the driving forces behind the transition from unicellular fungi to hyphal forms of growth, we develop a comparative model of osmotrophic resource acquisition. This predicts that whenever the local resource is immobile, hard-to-digest, and nutrient poor, hyphal osmotrophs outcompete motile or autolytic unicellular osmotrophs. This hyphal advantage arises because transporting nutrients via a contiguous cytoplasm enables continued exploitation of remaining resources after local depletion of essential nutrients, and more efficient use of costly exoenzymes. The model provides a mechanistic explanation for the origins of multicellular hyphal organisms, and explains why fungi, rather than unicellular bacteria, evolved to dominate decay of recalcitrant, nutrient poor substrates such as leaf litter or wood.
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spelling pubmed-72447132020-06-03 A mechanistic explanation of the transition to simple multicellularity in fungi Heaton, Luke L. M. Jones, Nick S. Fricker, Mark D. Nat Commun Article Development of multicellularity was one of the major transitions in evolution and occurred independently multiple times in algae, plants, animals, and fungi. However recent comparative genome analyses suggest that fungi followed a different route to other eukaryotic lineages. To understand the driving forces behind the transition from unicellular fungi to hyphal forms of growth, we develop a comparative model of osmotrophic resource acquisition. This predicts that whenever the local resource is immobile, hard-to-digest, and nutrient poor, hyphal osmotrophs outcompete motile or autolytic unicellular osmotrophs. This hyphal advantage arises because transporting nutrients via a contiguous cytoplasm enables continued exploitation of remaining resources after local depletion of essential nutrients, and more efficient use of costly exoenzymes. The model provides a mechanistic explanation for the origins of multicellular hyphal organisms, and explains why fungi, rather than unicellular bacteria, evolved to dominate decay of recalcitrant, nutrient poor substrates such as leaf litter or wood. Nature Publishing Group UK 2020-05-22 /pmc/articles/PMC7244713/ /pubmed/32444651 http://dx.doi.org/10.1038/s41467-020-16072-4 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Heaton, Luke L. M.
Jones, Nick S.
Fricker, Mark D.
A mechanistic explanation of the transition to simple multicellularity in fungi
title A mechanistic explanation of the transition to simple multicellularity in fungi
title_full A mechanistic explanation of the transition to simple multicellularity in fungi
title_fullStr A mechanistic explanation of the transition to simple multicellularity in fungi
title_full_unstemmed A mechanistic explanation of the transition to simple multicellularity in fungi
title_short A mechanistic explanation of the transition to simple multicellularity in fungi
title_sort mechanistic explanation of the transition to simple multicellularity in fungi
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7244713/
https://www.ncbi.nlm.nih.gov/pubmed/32444651
http://dx.doi.org/10.1038/s41467-020-16072-4
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