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Title: 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 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 ofmore » entire host-microbe complexes.« less

Authors:
 [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)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1213054
Grant/Contract Number:  
AC02-05CH11231; FC02-07ER64494
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 5; Journal Issue: 6; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Aylward, Frank O., Suen, Garret, Biedermann, Peter H. W., Adams, Aaron S., Scott, Jarrod J., Malfatti, Stephanie A., Glavina del Rio, Tijana, Tringe, Susannah G., Poulsen, Michael, Raffa, Kenneth F., Klepzig, Kier D., and Currie, Cameron R. Convergent bacterial microbiotas in the fungal agricultural systems of insects. United States: N. p., 2014. Web. doi:10.1128/mBio.02077-14.
Aylward, Frank O., Suen, Garret, Biedermann, Peter H. W., Adams, Aaron S., Scott, Jarrod J., Malfatti, Stephanie A., Glavina del Rio, Tijana, Tringe, Susannah G., Poulsen, Michael, Raffa, Kenneth F., Klepzig, Kier D., & Currie, Cameron R. Convergent bacterial microbiotas in the fungal agricultural systems of insects. United States. https://doi.org/10.1128/mBio.02077-14
Aylward, Frank O., Suen, Garret, Biedermann, Peter H. W., Adams, Aaron S., Scott, Jarrod J., Malfatti, Stephanie A., Glavina del Rio, Tijana, Tringe, Susannah G., Poulsen, Michael, Raffa, Kenneth F., Klepzig, Kier D., and Currie, Cameron R. Tue . "Convergent bacterial microbiotas in the fungal agricultural systems of insects". United States. https://doi.org/10.1128/mBio.02077-14. https://www.osti.gov/servlets/purl/1213054.
@article{osti_1213054,
title = {Convergent bacterial microbiotas in the fungal agricultural systems of insects},
author = {Aylward, Frank O. and Suen, Garret and Biedermann, Peter H. W. and Adams, Aaron S. and Scott, Jarrod J. and Malfatti, Stephanie A. and Glavina del Rio, Tijana and Tringe, Susannah G. and Poulsen, Michael and Raffa, Kenneth F. and Klepzig, Kier D. and Currie, Cameron R.},
abstractNote = {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.},
doi = {10.1128/mBio.02077-14},
journal = {mBio (Online)},
number = 6,
volume = 5,
place = {United States},
year = {Tue Nov 18 00:00:00 EST 2014},
month = {Tue Nov 18 00:00:00 EST 2014}
}

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Works referenced in this record:

Analysis of immune, microbiota and metabolome maturation in infants in a clinical trial of Lactobacillus paracasei CBA L74-fermented formula
journal, June 2020


Interactions in the microbiome: communities of organisms and communities of genes
journal, January 2014

  • Boon, Eva; Meehan, Conor J.; Whidden, Chris
  • FEMS Microbiology Reviews, Vol. 38, Issue 1
  • DOI: 10.1111/1574-6976.12035

The Pfam protein families database
journal, December 2007

  • Finn, R. D.; Tate, J.; Mistry, J.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm960

Yeast-like symbiotes as a sterol source in anobiid beetles (Coleoptera, Anobiidae): Possible metabolic pathways from fungal sterols to 7-dehydrocholesterol
journal, March 2003

  • Nasir, Habib; Noda, Hiroaki
  • Archives of Insect Biochemistry and Physiology, Vol. 52, Issue 4
  • DOI: 10.1002/arch.10079

Symbiotic Nitrogen Fixation in the Fungus Gardens of Leaf-Cutter Ants
journal, November 2009


Approximate Likelihood-Ratio Test for Branches: A Fast, Accurate, and Powerful Alternative
journal, August 2006


The Application of Ecological Theory Toward an Understanding of the Human Microbiome
journal, June 2012


Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes
journal, January 2014

  • Sanders, Jon G.; Powell, Scott; Kronauer, Daniel J. C.
  • Molecular Ecology, Vol. 23, Issue 6
  • DOI: 10.1111/mec.12611

Evolution of Mammals and Their Gut Microbes
journal, June 2008


Identification and phylogenetic sorting of bacterial lineages with universally conserved genes and proteins
journal, July 2004


Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

  • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
  • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
  • DOI: 10.1093/nar/25.17.3389

Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation
journal, October 2006


FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010


Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus
text, January 2009

  • Harris, R. N.; Brucker, R. M.; Walke, J. B.
  • Nature Publishing Group
  • DOI: 10.5167/uzh-19513

The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data
journal, January 2007

  • Cole, J. R.; Chai, B.; Farris, R. J.
  • Nucleic Acids Research, Vol. 35, Issue Database
  • DOI: 10.1093/nar/gkl889

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


The Evolution of Agriculture in Insects
journal, December 2005


Symbiosis
journal, October 2006


Normal gut microbiota modulates brain development and behavior
journal, January 2011

  • Heijtz, R. D.; Wang, S.; Anuar, F.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 7
  • DOI: 10.1073/pnas.1010529108

Symbioses: A Key Driver of Insect Physiological Processes, Ecological Interactions, Evolutionary Diversification, and Impacts on Humans
journal, February 2009

  • Klepzig, K. D.; Adams, A. S.; Handelsman, J.
  • Environmental Entomology, Vol. 38, Issue 1
  • DOI: 10.1603/022.038.0109

IMG/M: a data management and analysis system for metagenomes
journal, December 2007

  • Markowitz, V. M.; Ivanova, N. N.; Szeto, E.
  • Nucleic Acids Research, Vol. 36, Issue Database
  • DOI: 10.1093/nar/gkm869

From Structure to Function: the Ecology of Host-Associated Microbial Communities
journal, August 2010

  • Robinson, C. J.; Bohannan, B. J. M.; Young, V. B.
  • Microbiology and Molecular Biology Reviews, Vol. 74, Issue 3
  • DOI: 10.1128/MMBR.00014-10

Evolutionary Relationships of Wild Hominids Recapitulated by Gut Microbial Communities
journal, November 2010


Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009

  • Schloss, P. D.; Westcott, S. L.; Ryabin, T.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
  • DOI: 10.1128/AEM.01541-09

Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts
journal, June 2012

  • Fan, L.; Reynolds, D.; Liu, M.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 27
  • DOI: 10.1073/pnas.1203287109

An obesity-associated gut microbiome with increased capacity for energy harvest
journal, December 2006

  • Turnbaugh, Peter J.; Ley, Ruth E.; Mahowald, Michael A.
  • Nature, Vol. 444, Issue 7122
  • DOI: 10.1038/nature05414

Interactions Among Scolytid bark Beetles, Their Associated Fungi, and live host Conifers
journal, January 1997


Commensal bacteria play a role in mating preference of Drosophila melanogaster
journal, November 2010

  • Sharon, G.; Segal, D.; Ringo, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 46
  • DOI: 10.1073/pnas.1009906107

Insect Gut Bacterial Diversity Determined by Environmental Habitat, Diet, Developmental Stage, and Phylogeny of Host
journal, June 2014

  • Yun, Ji-Hyun; Roh, Seong Woon; Whon, Tae Woong
  • Applied and Environmental Microbiology, Vol. 80, Issue 17
  • DOI: 10.1128/AEM.01226-14

Bacterial Endosymbionts in the Gills of the Deep-Sea Wood-Boring Bivalves Xylophaga atlantica and Xylophaga washingtona
journal, April 1997

  • Distel, D. L.; Roberts, S. J.
  • The Biological Bulletin, Vol. 192, Issue 2
  • DOI: 10.2307/1542719

UCHIME improves sensitivity and speed of chimera detection
journal, June 2011


Cutaneous Bacteria of the Redback Salamander Prevent Morbidity Associated with a Lethal Disease
journal, June 2010


Basic Local Alignment Search Tool
journal, October 1990


Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm
journal, June 2010

  • Walter, J.; Britton, R. A.; Roos, S.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
  • DOI: 10.1073/pnas.1000099107

Ironing out the wrinkles in the rare biosphere through improved OTU clustering: Ironing out the wrinkles in the rare biosphere
journal, March 2010


Ecological and Evolutionary Forces Shaping Microbial Diversity in the Human Intestine
journal, February 2006


Convergent coevolution in the domestication of coral mushrooms by fungus–growing ants
journal, September 2004

  • Munkacsi, A. B.; Pan, J. J.; Villesen, P.
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 271, Issue 1550
  • DOI: 10.1098/rspb.2004.2759

Do diet and taxonomy influence insect gut bacterial communities?
journal, September 2012


Directional cDNA library construction assisted by the in vitro recombination reaction
journal, February 2001


Microbial community structure and functional properties in permanently and seasonally flooded areas in Poyang Lake
journal, March 2020


The microbial dimension in insect nutritional ecology
journal, February 2009


The Evolutionary Innovation of Nutritional Symbioses in Leaf-Cutter Ants
journal, January 2012


Mobyle: a new full web bioinformatics framework
journal, August 2009


Surveying the Microbiome of Ants: Comparing 454 Pyrosequencing with Traditional Methods To Uncover Bacterial Diversity
journal, November 2012

  • Kautz, Stefanie; Rubin, Benjamin E. R.; Russell, Jacob A.
  • Applied and Environmental Microbiology, Vol. 79, Issue 2
  • DOI: 10.1128/AEM.03107-12

Phymm and PhymmBL: metagenomic phylogenetic classification with interpolated Markov models
journal, August 2009

  • Brady, Arthur; Salzberg, Steven L.
  • Nature Methods, Vol. 6, Issue 9
  • DOI: 10.1038/nmeth.1358

Advances in Insect Phylogeny at the Dawn of the Postgenomic Era
journal, January 2012


Using the Metagenomics RAST Server (MG-RAST) for Analyzing Shotgun Metagenomes
journal, January 2010

  • Glass, E. M.; Wilkening, J.; Wilke, A.
  • Cold Spring Harbor Protocols, Vol. 2010, Issue 1
  • DOI: 10.1101/pdb.prot5368

Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus
journal, March 2009

  • Harris, Reid N.; Brucker, Robert M.; Walke, Jenifer B.
  • The ISME Journal, Vol. 3, Issue 7
  • DOI: 10.1038/ismej.2009.27

trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009


Diversity of locust gut bacteria protects against pathogen invasion
journal, December 2005


Microbiota regulates immune defense against respiratory tract influenza A virus infection
journal, March 2011

  • Ichinohe, T.; Pang, I. K.; Kumamoto, Y.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 13
  • DOI: 10.1073/pnas.1019378108

The Hologenomic Basis of Speciation: Gut Bacteria Cause Hybrid Lethality in the Genus Nasonia
journal, July 2013


Accurate determination of microbial diversity from 454 pyrosequencing data
journal, August 2009

  • Quince, Christopher; Lanzén, Anders; Curtis, Thomas P.
  • Nature Methods, Vol. 6, Issue 9
  • DOI: 10.1038/nmeth.1361

A new Generation of Homology Search Tools Based on Probabilistic Inference
conference, March 2012


Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite
journal, November 2007

  • Warnecke, Falk; Luginbühl, Peter; Ivanova, Natalia
  • Nature, Vol. 450, Issue 7169
  • DOI: 10.1038/nature06269

Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans
journal, May 2011


The COG database: new developments in phylogenetic classification of proteins from complete genomes
journal, January 2001


Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities
journal, September 2006

  • Martín, Héctor García; Ivanova, Natalia; Kunin, Victor
  • Nature Biotechnology, Vol. 24, Issue 10
  • DOI: 10.1038/nbt1247

Genome sequencing in microfabricated high-density picolitre reactors
journal, July 2005

  • Margulies, Marcel; Egholm, Michael; Altman, William E.
  • Nature, Vol. 437, Issue 7057, p. 376-380
  • DOI: 10.1038/nature03959

MAFFT version 5: improvement in accuracy of multiple sequence alignment
journal, January 2005


Genomic insights that advance the species definition for prokaryotes
journal, February 2005

  • Konstantinidis, K. T.; Tiedje, J. M.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 7
  • DOI: 10.1073/pnas.0409727102

An Insect Herbivore Microbiome with High Plant Biomass-Degrading Capacity
journal, September 2010


Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
journal, January 2011


Unearthing carrion beetles' microbiome: characterization of bacterial and fungal hindgut communities across the Silphidae
journal, September 2013

  • Kaltenpoth, Martin; Steiger, Sandra
  • Molecular Ecology, Vol. 23, Issue 6
  • DOI: 10.1111/mec.12469

Reducing the Effects of PCR Amplification and Sequencing Artifacts on 16S rRNA-Based Studies
journal, December 2011


Fungus-Growing Ants
journal, August 1966


Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens
journal, March 2012

  • Aylward, Frank O.; Burnum, Kristin E.; Scott, Jarrod J.
  • The ISME Journal, Vol. 6, Issue 9
  • DOI: 10.1038/ismej.2012.10

The Symbiotic Habit
book, December 2010


Works referencing / citing this record:

Impact of Rearing Conditions on the Ambrosia Beetle’s Microbiome
journal, December 2018

  • Ibarra-Juarez, Luis; Desgarennes, Damaris; Vázquez-Rosas-Landa, Mirna
  • Life, Vol. 8, Issue 4
  • DOI: 10.3390/life8040063

The fungal cultivar of leaf-cutter ants produces specific enzymes in response to different plant substrates
journal, October 2016

  • Khadempour, Lily; Burnum-Johnson, Kristin E.; Baker, Erin S.
  • Molecular Ecology, Vol. 25, Issue 22
  • DOI: 10.1111/mec.13872

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

  • Lee, Kevin M.; Adams, Madison; Klassen, Jonathan L.
  • PeerJ, Vol. 7
  • DOI: 10.7717/peerj.6414

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

  • Deveau, Aurélie; Bonito, Gregory; Uehling, Jessie
  • FEMS Microbiology Reviews, Vol. 42, Issue 3
  • DOI: 10.1093/femsre/fuy008

Assessment of a 16S rRNA amplicon Illumina sequencing procedure for studying the microbiome of a symbiont-rich aphid genus
journal, November 2015

  • Jousselin, E.; Clamens, A. -L.; Galan, M.
  • Molecular Ecology Resources, Vol. 16, Issue 3
  • DOI: 10.1111/1755-0998.12478

Diversity and Transmission of Gut Bacteria in Atta and Acromyrmex Leaf-Cutting Ants during Development
journal, October 2017

  • Zhukova, Mariya; Sapountzis, Panagiotis; Schiøtt, Morten
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.01942

Symbiont selection via alcohol benefits fungus farming by ambrosia beetles
journal, April 2018

  • Ranger, Christopher M.; Biedermann, Peter H. W.; Phuntumart, Vipaporn
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 17
  • DOI: 10.1073/pnas.1716852115

Draft genome sequences of Pantoea agglomerans and Pantoea vagans isolates associated with termites
journal, March 2016

  • Palmer, Marike; de Maayer, Pieter; Poulsen, Michael
  • Standards in Genomic Sciences, Vol. 11, Issue 1
  • DOI: 10.1186/s40793-016-0144-z

Profiling the metabolic signals involved in chemical communication between microbes using imaging mass spectrometry
journal, September 2016

  • Stasulli, Nikolas M.; Shank, Elizabeth A.
  • FEMS Microbiology Reviews, Vol. 40, Issue 6
  • DOI: 10.1093/femsre/fuw032

Pyrazines from bacteria and ants: convergent chemistry within an ecological niche
journal, February 2018

  • Silva-Junior, Eduardo A.; Ruzzini, Antonio C.; Paludo, Camila R.
  • Scientific Reports, Vol. 8, Issue 1
  • DOI: 10.1038/s41598-018-20953-6

Epibionts dominate metabolic functional potential of Trichodesmium colonies from the oligotrophic ocean
journal, May 2017

  • Frischkorn, Kyle R.; Rouco, Mónica; Van Mooy, Benjamin A. S.
  • The ISME Journal, Vol. 11, Issue 9
  • DOI: 10.1038/ismej.2017.74

Convergence between the microcosms of Southeast Asian and North American pitcher plants
journal, August 2018

  • Bittleston, Leonora S.; Wolock, Charles J.; Yahya, Bakhtiar E.
  • eLife, Vol. 7
  • DOI: 10.7554/elife.36741

Evaluation of DESS as a storage medium for microbial community analysis
posted_content, July 2018


Evaluation of DESS as a storage medium for microbial community analysis
posted_content, July 2018


High-Quality Draft Genome Sequences of Eight Bacteria Isolated from Fungus Gardens Grown by Trachymyrmex septentrionalis Ants
journal, July 2018

  • Kopac, Sarah; Beatty, Hannah; Gialopsos, Philip
  • Microbiology Resource Announcements, Vol. 7, Issue 2
  • DOI: 10.1128/mra.00871-18

Lignocellulose pretreatment in a fungus-cultivating termite
journal, April 2017

  • Li, Hongjie; Yelle, Daniel J.; Li, Chang
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 18
  • DOI: 10.1073/pnas.1618360114

Profiling the metabolic signals involved in chemical communication between microbes using imaging mass spectrometry
text, January 2016

  • M., Stasulli, Nikolas; A., Shank, Elizabeth
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/2qbd-g722

Variation in nest morphology, queen oviposition rates, and fungal species present in incipient colonies of the leaf-cutter ant Atta sexdens
journal, April 2019


Natural products from microbes associated with insects
journal, January 2016

  • Beemelmanns, Christine; Guo, Huijuan; Rischer, Maja
  • Beilstein Journal of Organic Chemistry, Vol. 12
  • DOI: 10.3762/bjoc.12.34

The evolution of abdominal microbiomes in fungus‐growing ants
journal, December 2018

  • Sapountzis, Panagiotis; Nash, David R.; Schiøtt, Morten
  • Molecular Ecology
  • DOI: 10.1111/mec.14931