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Title: Cellulose-Enriched Microbial Communities from Leaf-Cutter Ant (Atta colombica) Refuse Dumps Vary in Taxonomic Composition and Degradation Ability

Abstract

Deconstruction of the cellulose in plant cell walls is critical for carbon flow through ecosystems and for the production of sustainable cellulosic biofuels. Our understanding of cellulose deconstruction is largely limited to the study of microbes in isolation, but in nature, this process is driven by microbes within complex communities. In Neotropical forests, microbes in leaf-cutter ant refuse dumps are important for carbon turnover. These dumps consist of decaying plant material and a diverse bacterial community, as shown here by electron microscopy. To study the portion of the community capable of cellulose degradation, we performed enrichments on cellulose using material from five Atta colombica refuse dumps. The ability of enriched communities to degrade cellulose varied significantly across refuse dumps. 16S rRNA gene amplicon sequencing of enriched samples identified that the community structure correlated with refuse dump and with degradation ability. Overall, samples were dominated by Bacteroidetes, Gammaproteobacteria, and Betaproteobacteria. Half of abundant operational taxonomic units (OTUs) across samples were classified within general containing known cellulose degraders, including Acidovorax, the most abundant OTU detected across samples, which was positively correlated with cellulolytic ability. Lastly, a representative Acidovorax strain was isolated, but did not grow on cellulose alone. Phenotypic and compositional analysesmore » of enrichment cultures, such as those presented here, help link community composition with cellulolytic ability and provide insight into the complexity of community-based cellulose degradation.« less

Authors:
 [1];  [1];  [2];  [1];  [1];  [1];  [2];  [1]
  1. Univ. of Wisconsin-Madison, Madison, WI (United States)
  2. Univ. of Costa Rica, San Jose (Costa Rica)
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1255220
Grant/Contract Number:  
FC02-07ER64494; DGE-1256259; DEB-0747002
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 11; Journal Issue: 3; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Lewin, Gina R., Johnson, Amanda L., Soto, Rolando D. Moreira, Perry, Kailene, Book, Adam J., Horn, Heidi A., Pinto-Tomás, Adrián A., and Currie, Cameron R. Cellulose-Enriched Microbial Communities from Leaf-Cutter Ant (Atta colombica) Refuse Dumps Vary in Taxonomic Composition and Degradation Ability. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0151840.
Lewin, Gina R., Johnson, Amanda L., Soto, Rolando D. Moreira, Perry, Kailene, Book, Adam J., Horn, Heidi A., Pinto-Tomás, Adrián A., & Currie, Cameron R. Cellulose-Enriched Microbial Communities from Leaf-Cutter Ant (Atta colombica) Refuse Dumps Vary in Taxonomic Composition and Degradation Ability. United States. https://doi.org/10.1371/journal.pone.0151840
Lewin, Gina R., Johnson, Amanda L., Soto, Rolando D. Moreira, Perry, Kailene, Book, Adam J., Horn, Heidi A., Pinto-Tomás, Adrián A., and Currie, Cameron R. Mon . "Cellulose-Enriched Microbial Communities from Leaf-Cutter Ant (Atta colombica) Refuse Dumps Vary in Taxonomic Composition and Degradation Ability". United States. https://doi.org/10.1371/journal.pone.0151840. https://www.osti.gov/servlets/purl/1255220.
@article{osti_1255220,
title = {Cellulose-Enriched Microbial Communities from Leaf-Cutter Ant (Atta colombica) Refuse Dumps Vary in Taxonomic Composition and Degradation Ability},
author = {Lewin, Gina R. and Johnson, Amanda L. and Soto, Rolando D. Moreira and Perry, Kailene and Book, Adam J. and Horn, Heidi A. and Pinto-Tomás, Adrián A. and Currie, Cameron R.},
abstractNote = {Deconstruction of the cellulose in plant cell walls is critical for carbon flow through ecosystems and for the production of sustainable cellulosic biofuels. Our understanding of cellulose deconstruction is largely limited to the study of microbes in isolation, but in nature, this process is driven by microbes within complex communities. In Neotropical forests, microbes in leaf-cutter ant refuse dumps are important for carbon turnover. These dumps consist of decaying plant material and a diverse bacterial community, as shown here by electron microscopy. To study the portion of the community capable of cellulose degradation, we performed enrichments on cellulose using material from five Atta colombica refuse dumps. The ability of enriched communities to degrade cellulose varied significantly across refuse dumps. 16S rRNA gene amplicon sequencing of enriched samples identified that the community structure correlated with refuse dump and with degradation ability. Overall, samples were dominated by Bacteroidetes, Gammaproteobacteria, and Betaproteobacteria. Half of abundant operational taxonomic units (OTUs) across samples were classified within general containing known cellulose degraders, including Acidovorax, the most abundant OTU detected across samples, which was positively correlated with cellulolytic ability. Lastly, a representative Acidovorax strain was isolated, but did not grow on cellulose alone. Phenotypic and compositional analyses of enrichment cultures, such as those presented here, help link community composition with cellulolytic ability and provide insight into the complexity of community-based cellulose degradation.},
doi = {10.1371/journal.pone.0151840},
journal = {PLoS ONE},
number = 3,
volume = 11,
place = {United States},
year = {Mon Mar 21 00:00:00 EDT 2016},
month = {Mon Mar 21 00:00:00 EDT 2016}
}

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Glycoside Hydrolase Activities of Thermophilic Bacterial Consortia Adapted to Switchgrass
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Effect of Herbicides on Cellulose Decomposition by Sporocytophaga myxococcoides
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An Insect Herbivore Microbiome with High Plant Biomass-Degrading Capacity
journal, September 2010


Targeted Discovery of Glycoside Hydrolases from a Switchgrass-Adapted Compost Community
journal, January 2010


Microbial Community Structure of Leaf-Cutter Ant Fungus Gardens and Refuse Dumps
journal, March 2010


Effects of Biodiversity on Ecosystem Functioning: a Consensus of Current Knowledge
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Element and Energy Flows Through Colonies of the Leaf-Cutting Ant, Atta colombica, in Panama
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Do herbivores exert top‐down effects in Neotropical savannas? Estimates of biomass consumption by leaf‐cutter ants
journal, January 2008

  • Costa, Alan N.; Vasconcelos, Heraldo L.; Vieira‐Neto, Ernane H. M.
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Bacterial genomes: what they teach us about cellulose degradation
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