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...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2014-12-01
|
| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02077-14 |
| _version_ | 1818822498984132608 |
|---|---|
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-18T23:25:03Z |
| format | Article |
| id | doaj.art-438ea98dd8a14a00a1227442ac49e358 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-18T23:25:03Z |
| publishDate | 2014-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-438ea98dd8a14a00a1227442ac49e3582022-12-21T20:47:49ZengAmerican Society for MicrobiologymBio2150-75112014-12-015610.1128/mBio.02077-14Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of InsectsFrank O. Aylward0Garret Suen1Peter H. W. Biedermann2Aaron S. Adams3Jarrod J. Scott4Stephanie A. Malfatti5Tijana Glavina del Rio6Susannah G. Tringe7Michael Poulsen8Kenneth F. Raffa9Kier D. Klepzig10Cameron R. Currie11Department of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USADepartment of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USAInsect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, Jena, GermanyDepartment of Entomology, University of Wisconsin—Madison, Madison, Wisconsin, USADepartment of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USADepartment of Energy Joint Genome Institute, Walnut Creek, California, USADepartment of Energy Joint Genome Institute, Walnut Creek, California, USADepartment of Energy Joint Genome Institute, Walnut Creek, California, USASection for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, DenmarkDepartment of Entomology, University of Wisconsin—Madison, Madison, Wisconsin, USAUSDA Forest Service, Southern Research Station, Asheville, North Carolina, USADepartment of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/mBio.02077-14 |
| spellingShingle | 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 mBio |
| title | 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_short | Convergent Bacterial Microbiotas in the Fungal Agricultural Systems of Insects |
| title_sort | convergent bacterial microbiotas in the fungal agricultural systems of insects |
| url | https://journals.asm.org/doi/10.1128/mBio.02077-14 |
| work_keys_str_mv | AT frankoaylward convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT garretsuen convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT peterhwbiedermann convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT aaronsadams convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT jarrodjscott convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT stephanieamalfatti convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT tijanaglavinadelrio convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT susannahgtringe convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT michaelpoulsen convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT kennethfraffa convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT kierdklepzig convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects AT cameronrcurrie convergentbacterialmicrobiotasinthefungalagriculturalsystemsofinsects |