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Research Article

Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects

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
Arturo Casadevall, Editor
Frank O. Aylward
aDepartment of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
bDepartment of Energy Great Lakes Bioenergy Research Center, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Garret Suen
aDepartment of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Peter H. W. Biedermann
cInsect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, Jena, Germany
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Aaron S. Adams
dDepartment of Entomology, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Jarrod J. Scott
aDepartment of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
bDepartment of Energy Great Lakes Bioenergy Research Center, University of Wisconsin—Madison, Madison, Wisconsin, USA
eSmithsonian Tropical Research Institute, Balboa, Ancon, Panama
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Stephanie A. Malfatti
fDepartment of Energy Joint Genome Institute, Walnut Creek, California, USA
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Tijana Glavina del Rio
fDepartment of Energy Joint Genome Institute, Walnut Creek, California, USA
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Susannah G. Tringe
fDepartment of Energy Joint Genome Institute, Walnut Creek, California, USA
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Michael Poulsen
gSection for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark
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Kenneth F. Raffa
dDepartment of Entomology, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Kier D. Klepzig
hUSDA Forest Service, Southern Research Station, Asheville, North Carolina, USA
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Cameron R. Currie
aDepartment of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USA
bDepartment of Energy Great Lakes Bioenergy Research Center, University of Wisconsin—Madison, Madison, Wisconsin, USA
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Arturo Casadevall
Albert Einstein College of Medicine
Roles: Editor
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DOI: 10.1128/mBio.02077-14
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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.

FOOTNOTES

    • Received 8 October 2014
    • Accepted 29 October 2014
    • Published 18 November 2014
  • Copyright © 2014 Aylward et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects
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
mBio Nov 2014, 5 (6) e02077-14; DOI: 10.1128/mBio.02077-14

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Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects
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
mBio Nov 2014, 5 (6) e02077-14; DOI: 10.1128/mBio.02077-14
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