Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System

ABSTRACT Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist...

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Autores principales:	Charlotte B. Francoeur, Lily Khadempour, Rolando D. Moreira-Soto, Kirsten Gotting, Adam J. Book, Adrián A. Pinto-Tomás, Ken Keefover-Ring, Cameron R. Currie
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	attine detoxification fungus garden leaf-cutter ant symbiosis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4564bbf117fe4dbaa2002b08dfaa2176
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spelling	oai:doaj.org-article:4564bbf117fe4dbaa2002b08dfaa21762021-11-15T16:19:07ZBacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System10.1128/mBio.02146-202150-7511https://doaj.org/article/4564bbf117fe4dbaa2002b08dfaa21762020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02146-20https://doaj.org/toc/2150-7511ABSTRACT Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems and which degrade the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within fungus gardens. In this study, we investigated the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome P450 enzymes and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we showed that some of these degradation genes are expressed in situ. Most of the bacterial isolates grew unhindered in the presence of PSCs and, using gas chromatography-mass spectrometry (GC-MS), we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that subcolonies of fungus gardens reduced α-pinene and linalool over a 36-h period, while L. gongylophorus strains alone reduced only linalool. Overall, our results reveal that the bacterial communities in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system. IMPORTANCE Leaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut, composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their roles in the detoxification of plant secondary compounds. In this study, we assessed if the bacterial communities associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus. Our findings suggest that the fungus garden and its associated microbial community influence the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores.Charlotte B. FrancoeurLily KhadempourRolando D. Moreira-SotoKirsten GottingAdam J. BookAdrián A. Pinto-TomásKen Keefover-RingCameron R. CurrieAmerican Society for Microbiologyarticleattinedetoxificationfungus gardenleaf-cutter antsymbiosisMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	attine detoxification fungus garden leaf-cutter ant symbiosis Microbiology QR1-502
spellingShingle	attine detoxification fungus garden leaf-cutter ant symbiosis Microbiology QR1-502 Charlotte B. Francoeur Lily Khadempour Rolando D. Moreira-Soto Kirsten Gotting Adam J. Book Adrián A. Pinto-Tomás Ken Keefover-Ring Cameron R. Currie Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System
description	ABSTRACT Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems and which degrade the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within fungus gardens. In this study, we investigated the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome P450 enzymes and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we showed that some of these degradation genes are expressed in situ. Most of the bacterial isolates grew unhindered in the presence of PSCs and, using gas chromatography-mass spectrometry (GC-MS), we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that subcolonies of fungus gardens reduced α-pinene and linalool over a 36-h period, while L. gongylophorus strains alone reduced only linalool. Overall, our results reveal that the bacterial communities in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system. IMPORTANCE Leaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut, composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their roles in the detoxification of plant secondary compounds. In this study, we assessed if the bacterial communities associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus. Our findings suggest that the fungus garden and its associated microbial community influence the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores.
format	article
author	Charlotte B. Francoeur Lily Khadempour Rolando D. Moreira-Soto Kirsten Gotting Adam J. Book Adrián A. Pinto-Tomás Ken Keefover-Ring Cameron R. Currie
author_facet	Charlotte B. Francoeur Lily Khadempour Rolando D. Moreira-Soto Kirsten Gotting Adam J. Book Adrián A. Pinto-Tomás Ken Keefover-Ring Cameron R. Currie
author_sort	Charlotte B. Francoeur
title	Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System
title_short	Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System
title_full	Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System
title_fullStr	Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System
title_full_unstemmed	Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System
title_sort	bacteria contribute to plant secondary compound degradation in a generalist herbivore system
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/4564bbf117fe4dbaa2002b08dfaa2176
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Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System

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