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A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers

While ants are dominant consumers in terrestrial habitats, only the leafcutters practice herbivory. Leafcutters do this by provisioning a fungal cultivar (Leucoagaricus gongylophorus) with freshly cut plant fragments and harnessing its metabolic machinery to convert plant mulch into edible fungal ti...

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Autores principales: Conlon, Benjamin H., O'Tuama, David, Michelsen, Anders, Crumière, Antonin J. J., Shik, Jonathan Z.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9019514/
https://www.ncbi.nlm.nih.gov/pubmed/35440234
http://dx.doi.org/10.1098/rsbl.2022.0022
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author Conlon, Benjamin H.
O'Tuama, David
Michelsen, Anders
Crumière, Antonin J. J.
Shik, Jonathan Z.
author_facet Conlon, Benjamin H.
O'Tuama, David
Michelsen, Anders
Crumière, Antonin J. J.
Shik, Jonathan Z.
author_sort Conlon, Benjamin H.
collection PubMed
description While ants are dominant consumers in terrestrial habitats, only the leafcutters practice herbivory. Leafcutters do this by provisioning a fungal cultivar (Leucoagaricus gongylophorus) with freshly cut plant fragments and harnessing its metabolic machinery to convert plant mulch into edible fungal tissue (hyphae and swollen hyphal cells called gongylidia). The cultivar is known to degrade cellulose, but whether it assimilates this ubiquitous but recalcitrant molecule into its nutritional reward structures is unknown. We use in vitro experiments with isotopically labelled cellulose to show that fungal cultures from an Atta colombica leafcutter colony convert cellulose-derived carbon into gongylidia, even when potential bacterial symbionts are excluded. A laboratory feeding experiment showed that cellulose assimilation also occurs in vivo in A. colombica colonies. Analyses of publicly available transcriptomic data further identified a complete, constitutively expressed, cellulose-degradation pathway in the fungal cultivar. Confirming leafcutters use cellulose as a food source sheds light on the eco-evolutionary success of these important herbivores.
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spelling pubmed-90195142022-04-21 A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers Conlon, Benjamin H. O'Tuama, David Michelsen, Anders Crumière, Antonin J. J. Shik, Jonathan Z. Biol Lett Physiology While ants are dominant consumers in terrestrial habitats, only the leafcutters practice herbivory. Leafcutters do this by provisioning a fungal cultivar (Leucoagaricus gongylophorus) with freshly cut plant fragments and harnessing its metabolic machinery to convert plant mulch into edible fungal tissue (hyphae and swollen hyphal cells called gongylidia). The cultivar is known to degrade cellulose, but whether it assimilates this ubiquitous but recalcitrant molecule into its nutritional reward structures is unknown. We use in vitro experiments with isotopically labelled cellulose to show that fungal cultures from an Atta colombica leafcutter colony convert cellulose-derived carbon into gongylidia, even when potential bacterial symbionts are excluded. A laboratory feeding experiment showed that cellulose assimilation also occurs in vivo in A. colombica colonies. Analyses of publicly available transcriptomic data further identified a complete, constitutively expressed, cellulose-degradation pathway in the fungal cultivar. Confirming leafcutters use cellulose as a food source sheds light on the eco-evolutionary success of these important herbivores. The Royal Society 2022-04-20 /pmc/articles/PMC9019514/ /pubmed/35440234 http://dx.doi.org/10.1098/rsbl.2022.0022 Text en © 2022 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Physiology
Conlon, Benjamin H.
O'Tuama, David
Michelsen, Anders
Crumière, Antonin J. J.
Shik, Jonathan Z.
A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers
title A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers
title_full A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers
title_fullStr A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers
title_full_unstemmed A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers
title_short A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers
title_sort fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9019514/
https://www.ncbi.nlm.nih.gov/pubmed/35440234
http://dx.doi.org/10.1098/rsbl.2022.0022
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