Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects

ABSTRACT The ability to cultivate food is an innovation that has produced some of the most successful ecological strategies on the planet. Although most well recognized in humans, where agriculture represents a defining feature of civilization, species of ants, beetles, and termites have also indepe...

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Autores principales:	Frank O. Aylward, Garret Suen, Peter H. W. Biedermann, Aaron S. Adams, Jarrod J. Scott, Stephanie A. Malfatti, Tijana Glavina del Rio, Susannah G. Tringe, Michael Poulsen, Kenneth F. Raffa, Kier D. Klepzig, Cameron R. Currie
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/438ea98dd8a14a00a1227442ac49e358
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spelling	oai:doaj.org-article:438ea98dd8a14a00a1227442ac49e3582021-11-15T15:47:03ZConvergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects10.1128/mBio.02077-142150-7511https://doaj.org/article/438ea98dd8a14a00a1227442ac49e3582014-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02077-14https://doaj.org/toc/2150-7511ABSTRACT The ability to cultivate food is an innovation that has produced some of the most successful ecological strategies on the planet. Although most well recognized in humans, where agriculture represents a defining feature of civilization, species of ants, beetles, and termites have also independently evolved symbioses with fungi that they cultivate for food. Despite occurring across divergent insect and fungal lineages, the fungivorous niches of these insects are remarkably similar, indicating convergent evolution toward this successful ecological strategy. Here, we characterize the microbiota of ants, beetles, and termites engaged in nutritional symbioses with fungi to define the bacterial groups associated with these prominent herbivores and forest pests. Using culture-independent techniques and the in silico reconstruction of 37 composite genomes of dominant community members, we demonstrate that different insect-fungal symbioses that collectively shape ecosystems worldwide have highly similar bacterial microbiotas comprised primarily of the genera Enterobacter, Rahnella, and Pseudomonas. Although these symbioses span three orders of insects and two phyla of fungi, we show that they are associated with bacteria sharing high whole-genome nucleotide identity. Due to the fine-scale correspondence of the bacterial microbiotas of insects engaged in fungal symbioses, our findings indicate that this represents an example of convergence of entire host-microbe complexes. IMPORTANCE The cultivation of fungi for food is a behavior that has evolved independently in ants, beetles, and termites and has enabled many species of these insects to become ecologically important and widely distributed herbivores and forest pests. Although the primary fungal cultivars of these insects have been studied for decades, comparatively little is known of their bacterial microbiota. In this study, we show that diverse fungus-growing insects are associated with a common bacterial community composed of the same dominant members. Furthermore, by demonstrating that many of these bacteria have high whole-genome similarity across distantly related insect hosts that reside thousands of miles apart, we show that these bacteria are an important and underappreciated feature of diverse fungus-growing insects. Because of the similarities in the agricultural lifestyles of these insects, this is an example of convergence between both the life histories of the host insects and their symbiotic microbiota.Frank O. AylwardGarret SuenPeter H. W. BiedermannAaron S. AdamsJarrod J. ScottStephanie A. MalfattiTijana Glavina del RioSusannah G. TringeMichael PoulsenKenneth F. RaffaKier D. KlepzigCameron R. CurrieAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 6 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Frank O. Aylward Garret Suen Peter H. W. Biedermann Aaron S. Adams Jarrod J. Scott Stephanie A. Malfatti Tijana Glavina del Rio Susannah G. Tringe Michael Poulsen Kenneth F. Raffa Kier D. Klepzig Cameron R. Currie Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects
description	ABSTRACT The ability to cultivate food is an innovation that has produced some of the most successful ecological strategies on the planet. Although most well recognized in humans, where agriculture represents a defining feature of civilization, species of ants, beetles, and termites have also independently evolved symbioses with fungi that they cultivate for food. Despite occurring across divergent insect and fungal lineages, the fungivorous niches of these insects are remarkably similar, indicating convergent evolution toward this successful ecological strategy. Here, we characterize the microbiota of ants, beetles, and termites engaged in nutritional symbioses with fungi to define the bacterial groups associated with these prominent herbivores and forest pests. Using culture-independent techniques and the in silico reconstruction of 37 composite genomes of dominant community members, we demonstrate that different insect-fungal symbioses that collectively shape ecosystems worldwide have highly similar bacterial microbiotas comprised primarily of the genera Enterobacter, Rahnella, and Pseudomonas. Although these symbioses span three orders of insects and two phyla of fungi, we show that they are associated with bacteria sharing high whole-genome nucleotide identity. Due to the fine-scale correspondence of the bacterial microbiotas of insects engaged in fungal symbioses, our findings indicate that this represents an example of convergence of entire host-microbe complexes. IMPORTANCE The cultivation of fungi for food is a behavior that has evolved independently in ants, beetles, and termites and has enabled many species of these insects to become ecologically important and widely distributed herbivores and forest pests. Although the primary fungal cultivars of these insects have been studied for decades, comparatively little is known of their bacterial microbiota. In this study, we show that diverse fungus-growing insects are associated with a common bacterial community composed of the same dominant members. Furthermore, by demonstrating that many of these bacteria have high whole-genome similarity across distantly related insect hosts that reside thousands of miles apart, we show that these bacteria are an important and underappreciated feature of diverse fungus-growing insects. Because of the similarities in the agricultural lifestyles of these insects, this is an example of convergence between both the life histories of the host insects and their symbiotic microbiota.
format	article
author	Frank O. Aylward Garret Suen Peter H. W. Biedermann Aaron S. Adams Jarrod J. Scott Stephanie A. Malfatti Tijana Glavina del Rio Susannah G. Tringe Michael Poulsen Kenneth F. Raffa Kier D. Klepzig Cameron R. Currie
author_facet	Frank O. Aylward Garret Suen Peter H. W. Biedermann Aaron S. Adams Jarrod J. Scott Stephanie A. Malfatti Tijana Glavina del Rio Susannah G. Tringe Michael Poulsen Kenneth F. Raffa Kier D. Klepzig Cameron R. Currie
author_sort	Frank O. Aylward
title	Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects
title_short	Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects
title_full	Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects
title_fullStr	Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects
title_full_unstemmed	Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects
title_sort	convergent bacterial microbiotas in the fungal agricultural systems of insects
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/438ea98dd8a14a00a1227442ac49e358
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Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects

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