From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem

ABSTRACT Lipids are essential to all living organisms, as an energy source, as an important cellular structural component, and as a communication tool. In this study, we used global lipidomic methods to evaluate the lipids in leaf-cutter ant fungal gardens. Leaf-cutter ants and their coevolved funga...

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Autores principales:	Lily Khadempour, Jennifer E. Kyle, Bobbie-Jo M. Webb-Robertson, Carrie D. Nicora, Francesca B. Smith, Richard D. Smith, Mary S. Lipton, Cameron R. Currie, Erin S. Baker, Kristin E. Burnum-Johnson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	18:2 18:3 alpha-linolenic acid fungal garden ecosystem interkingdom communication leaf-cutter ants Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8344f5fe2d614af79449d48a7da4c8a0
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spelling	oai:doaj.org-article:8344f5fe2d614af79449d48a7da4c8a02021-12-02T19:36:39ZFrom Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem10.1128/mSystems.01307-202379-5077https://doaj.org/article/8344f5fe2d614af79449d48a7da4c8a02021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01307-20https://doaj.org/toc/2379-5077ABSTRACT Lipids are essential to all living organisms, as an energy source, as an important cellular structural component, and as a communication tool. In this study, we used global lipidomic methods to evaluate the lipids in leaf-cutter ant fungal gardens. Leaf-cutter ants and their coevolved fungal cultivar, Leucoagaricus gongylophorus, are a model mutualistic system. The fungus enzymatically digests fresh plant material that the ants cut and deliver, converting energy and nutrients from plants and providing them to the ants through specialized hyphal swellings called gongylidia. Using combined liquid chromatography, ion mobility spectrometry, and tandem mass spectrometry, we evaluated differences between the molecular species of lipids in the leaf-cutter ant fungal garden ecosystem. This lipidomic study characterized leaves that are fed to the gardens, gongylidia that are produced by the fungus to feed the ants, and spatially resolved regions of the fungal garden through stages of leaf degradation. Lipids containing alpha-linolenic acid (18:3) were enriched in leaves and the top of the gardens but not dominant in the middle or bottom regions. Gongylidia were dominated by lipids containing linoleic acid (18:2). To evaluate the communicative potential of the lipids in fungal gardens, we conducted a behavioral experiment that showed Atta leaf-cutter ants responded differently to 18:3 and 18:2 fatty acids, with aggression toward 18:3 and attraction for 18:2. This work demonstrates the role of lipids in both the transfer of energy and as an interkingdom communication tool in leaf-cutter ant fungal gardens. IMPORTANCE In this work, we examined the role of lipids in the mutualism between leaf-cutter ants and fungus. These ants cut fresh leaf material, which they provide to their fungal cultivar, that converts energy and nutrients from the plants and provides it to the ants in specialized hyphal swellings called gongylidia. This work constitutes the first example of a global lipidomics study of a symbiotic system and provides insights as to how the fungus modifies plant lipids into a usable source for the ants. Through a behavioral experiment, this work also demonstrates how lipids can be used as an interkingdom communication tool, in this case, as an attractant rather than as a repellant, which is more often seen. Author Video: An author video summary of this article is available.Lily KhadempourJennifer E. KyleBobbie-Jo M. Webb-RobertsonCarrie D. NicoraFrancesca B. SmithRichard D. SmithMary S. LiptonCameron R. CurrieErin S. BakerKristin E. Burnum-JohnsonAmerican Society for Microbiologyarticle18:218:3alpha-linolenic acidfungal garden ecosysteminterkingdom communicationleaf-cutter antsMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	18:2 18:3 alpha-linolenic acid fungal garden ecosystem interkingdom communication leaf-cutter ants Microbiology QR1-502
spellingShingle	18:2 18:3 alpha-linolenic acid fungal garden ecosystem interkingdom communication leaf-cutter ants Microbiology QR1-502 Lily Khadempour Jennifer E. Kyle Bobbie-Jo M. Webb-Robertson Carrie D. Nicora Francesca B. Smith Richard D. Smith Mary S. Lipton Cameron R. Currie Erin S. Baker Kristin E. Burnum-Johnson From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem
description	ABSTRACT Lipids are essential to all living organisms, as an energy source, as an important cellular structural component, and as a communication tool. In this study, we used global lipidomic methods to evaluate the lipids in leaf-cutter ant fungal gardens. Leaf-cutter ants and their coevolved fungal cultivar, Leucoagaricus gongylophorus, are a model mutualistic system. The fungus enzymatically digests fresh plant material that the ants cut and deliver, converting energy and nutrients from plants and providing them to the ants through specialized hyphal swellings called gongylidia. Using combined liquid chromatography, ion mobility spectrometry, and tandem mass spectrometry, we evaluated differences between the molecular species of lipids in the leaf-cutter ant fungal garden ecosystem. This lipidomic study characterized leaves that are fed to the gardens, gongylidia that are produced by the fungus to feed the ants, and spatially resolved regions of the fungal garden through stages of leaf degradation. Lipids containing alpha-linolenic acid (18:3) were enriched in leaves and the top of the gardens but not dominant in the middle or bottom regions. Gongylidia were dominated by lipids containing linoleic acid (18:2). To evaluate the communicative potential of the lipids in fungal gardens, we conducted a behavioral experiment that showed Atta leaf-cutter ants responded differently to 18:3 and 18:2 fatty acids, with aggression toward 18:3 and attraction for 18:2. This work demonstrates the role of lipids in both the transfer of energy and as an interkingdom communication tool in leaf-cutter ant fungal gardens. IMPORTANCE In this work, we examined the role of lipids in the mutualism between leaf-cutter ants and fungus. These ants cut fresh leaf material, which they provide to their fungal cultivar, that converts energy and nutrients from the plants and provides it to the ants in specialized hyphal swellings called gongylidia. This work constitutes the first example of a global lipidomics study of a symbiotic system and provides insights as to how the fungus modifies plant lipids into a usable source for the ants. Through a behavioral experiment, this work also demonstrates how lipids can be used as an interkingdom communication tool, in this case, as an attractant rather than as a repellant, which is more often seen. Author Video: An author video summary of this article is available.
format	article
author	Lily Khadempour Jennifer E. Kyle Bobbie-Jo M. Webb-Robertson Carrie D. Nicora Francesca B. Smith Richard D. Smith Mary S. Lipton Cameron R. Currie Erin S. Baker Kristin E. Burnum-Johnson
author_facet	Lily Khadempour Jennifer E. Kyle Bobbie-Jo M. Webb-Robertson Carrie D. Nicora Francesca B. Smith Richard D. Smith Mary S. Lipton Cameron R. Currie Erin S. Baker Kristin E. Burnum-Johnson
author_sort	Lily Khadempour
title	From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem
title_short	From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem
title_full	From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem
title_fullStr	From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem
title_full_unstemmed	From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem
title_sort	from plants to ants: fungal modification of leaf lipids for nutrition and communication in the leaf-cutter ant fungal garden ecosystem
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/8344f5fe2d614af79449d48a7da4c8a0
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From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem

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