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Title: Convergent bacterial microbiotas in the fungal agricultural systems of insects

Journal Article · · mBio (Online)
 [1];  [1];  [2];  [1];  [3];  [4];  [4];  [4];  [5];  [1];  [6];  [1]
  1. Univ. of Wisconsin, Madison, WI (United States)
  2. Max Planck Institute for Chemical Ecology, Jena (Germany)
  3. Univ. of Wisconsin, Madison, WI (United States); Smithsonian Tropical Research Institute, Balboa, Ancon (Panama)
  4. Dept. of Energy Joint Genome Institute, Walnut Creek, CA (United States)
  5. Univ. of Copenhagen, Copenhagen (Denmark)
  6. Southern Research Station, Asheville, NC (United States)

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231; FC02-07ER64494
OSTI ID:
1213054
Journal Information:
mBio (Online), Vol. 5, Issue 6; ISSN 2150-7511
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 71 works
Citation information provided by
Web of Science

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Cited By (25)

Impact of Rearing Conditions on the Ambrosia Beetle’s Microbiome journal December 2018
The fungal cultivar of leaf-cutter ants produces specific enzymes in response to different plant substrates journal October 2016
A census-based estimate of Earth's bacterial and archaeal diversity journal February 2019
Evaluation of DESS as a storage medium for microbial community analysis journal January 2019
Evolution of High Cellulolytic Activity in Symbiotic Streptomyces through Selection of Expanded Gene Content and Coordinated Gene Expression journal June 2016
Antimicrobial activity and carbohydrate metabolism in the bacterial metagenome of the soil-living invertebrate Folsomia candida journal May 2019
Bacterial–fungal interactions: ecology, mechanisms and challenges journal February 2018
Assessment of a 16S rRNA amplicon Illumina sequencing procedure for studying the microbiome of a symbiont-rich aphid genus journal November 2015
Diversity and Transmission of Gut Bacteria in Atta and Acromyrmex Leaf-Cutting Ants during Development journal October 2017
Symbiont selection via alcohol benefits fungus farming by ambrosia beetles journal April 2018
Draft genome sequences of Pantoea agglomerans and Pantoea vagans isolates associated with termites journal March 2016
Profiling the metabolic signals involved in chemical communication between microbes using imaging mass spectrometry journal September 2016
Pyrazines from bacteria and ants: convergent chemistry within an ecological niche journal February 2018
Epibionts dominate metabolic functional potential of Trichodesmium colonies from the oligotrophic ocean journal May 2017
Convergence between the microcosms of Southeast Asian and North American pitcher plants journal August 2018
Evaluation of DESS as a storage medium for microbial community analysis posted_content July 2018
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Bacterial and Fungal Midgut Community Dynamics and Transfer Between Mother and Brood in the Asian Longhorned Beetle (Anoplophora glabripennis), an Invasive Xylophage journal June 2018
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Lignocellulose pretreatment in a fungus-cultivating termite journal April 2017
Enrichment and Broad Representation of Plant Biomass-Degrading Enzymes in the Specialized Hyphal Swellings of Leucoagaricus gongylophorus, the Fungal Symbiont of Leaf-Cutter Ants journal August 2015
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