Enrichment and broad representation of plant biomass-degrading enzymes in the specialized hyphal swellings of Leucoagaricus gongylophorus, the fungal symbiont of leaf-cutter ants
Abstract
Leaf-cutter ants are prolific and conspicuous constituents of Neotropical ecosystems that derive energy from specialized fungus gardens they cultivate using prodigious amounts of foliar biomass. The basidiomycetous cultivar of the ants, Leucoagaricus gongylophorus, produces specialized hyphal swellings called gongylidia that serve as the primary food source of ant colonies. Gongylidia also contain plant biomass-degrading enzymes that become concentrated in ant digestive tracts and are deposited within fecal droplets onto fresh foliar material as ants incorporate it into the fungus garden. Although the enzymes concentrated by L. gongylophorus within gongylidia are thought to be critical to the initial degradation of plant biomass, only a few enzymes present in these hyphal swellings have been identified. Here we use proteomic methods to identify proteins present in the gongylidia of three Atta cephalotes colonies. Our results demonstrate that a diverse but consistent set of enzymes is present in gongylidia, including numerous plant biomass-degrading enzymes likely involved in the degradation of polysaccharides, plant toxins, and proteins. Overall, gongylidia contained over three quarters of all biomass-degrading enzymes identified in the L. gongylophorus genome, demonstrating that the majority of the enzymes produced by this fungus for biomass breakdown are ingested by the ants. We also identify amore »
- Authors:
-
- University of Wisconson-Madison, Madison, WI (United States). Department of Bacteriology; University of Hawaii, Manoa, Honolulu, HI (United States). Cemter for Microbial Oceanography Research and Education.
- University of Wisconson-Madison, Madison, WI (United States). Department of Bacteriology.
- University of Wisconson-Madison, Madison, WI (United States). Department of Bacteriology.
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Divisio
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division; University of Oklahoma, Norman, OK (United States). Department of Chemistry and Biochemistr
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biological Sciences Division.
- Smithsonian National Museum of Natural History, Washington, DC (United States)
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
- OSTI Identifier:
- 1213522
- Grant/Contract Number:
- AC05-76RL01830; FC02-07ER64494
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 8; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; fungi; ants; proteases; fungal genomics; biomass (ecology); proteomics; symbiosis; fungiculture
Citation Formats
Aylward, Frank O., Khadempour, Lily, Tremmel, Daniel M., McDonald, Bradon R., Nicora, Carrie D., Wu, Si, Moore, Ronald J., Orton, Daniel J., Monroe, Matthew E., Piehowski, Paul D., Purvine, Samuel O., Smith, Richard D., Lipton, Mary S., Burnum-Johnson, Kristin E., Currie, Cameron R., and Brady, Sean. Enrichment and broad representation of plant biomass-degrading enzymes in the specialized hyphal swellings of Leucoagaricus gongylophorus, the fungal symbiont of leaf-cutter ants. United States: N. p., 2015.
Web. doi:10.1371/journal.pone.0134752.
Aylward, Frank O., Khadempour, Lily, Tremmel, Daniel M., McDonald, Bradon R., Nicora, Carrie D., Wu, Si, Moore, Ronald J., Orton, Daniel J., Monroe, Matthew E., Piehowski, Paul D., Purvine, Samuel O., Smith, Richard D., Lipton, Mary S., Burnum-Johnson, Kristin E., Currie, Cameron R., & Brady, Sean. Enrichment and broad representation of plant biomass-degrading enzymes in the specialized hyphal swellings of Leucoagaricus gongylophorus, the fungal symbiont of leaf-cutter ants. United States. https://doi.org/10.1371/journal.pone.0134752
Aylward, Frank O., Khadempour, Lily, Tremmel, Daniel M., McDonald, Bradon R., Nicora, Carrie D., Wu, Si, Moore, Ronald J., Orton, Daniel J., Monroe, Matthew E., Piehowski, Paul D., Purvine, Samuel O., Smith, Richard D., Lipton, Mary S., Burnum-Johnson, Kristin E., Currie, Cameron R., and Brady, Sean. Fri .
"Enrichment and broad representation of plant biomass-degrading enzymes in the specialized hyphal swellings of Leucoagaricus gongylophorus, the fungal symbiont of leaf-cutter ants". United States. https://doi.org/10.1371/journal.pone.0134752. https://www.osti.gov/servlets/purl/1213522.
@article{osti_1213522,
title = {Enrichment and broad representation of plant biomass-degrading enzymes in the specialized hyphal swellings of Leucoagaricus gongylophorus, the fungal symbiont of leaf-cutter ants},
author = {Aylward, Frank O. and Khadempour, Lily and Tremmel, Daniel M. and McDonald, Bradon R. and Nicora, Carrie D. and Wu, Si and Moore, Ronald J. and Orton, Daniel J. and Monroe, Matthew E. and Piehowski, Paul D. and Purvine, Samuel O. and Smith, Richard D. and Lipton, Mary S. and Burnum-Johnson, Kristin E. and Currie, Cameron R. and Brady, Sean},
abstractNote = {Leaf-cutter ants are prolific and conspicuous constituents of Neotropical ecosystems that derive energy from specialized fungus gardens they cultivate using prodigious amounts of foliar biomass. The basidiomycetous cultivar of the ants, Leucoagaricus gongylophorus, produces specialized hyphal swellings called gongylidia that serve as the primary food source of ant colonies. Gongylidia also contain plant biomass-degrading enzymes that become concentrated in ant digestive tracts and are deposited within fecal droplets onto fresh foliar material as ants incorporate it into the fungus garden. Although the enzymes concentrated by L. gongylophorus within gongylidia are thought to be critical to the initial degradation of plant biomass, only a few enzymes present in these hyphal swellings have been identified. Here we use proteomic methods to identify proteins present in the gongylidia of three Atta cephalotes colonies. Our results demonstrate that a diverse but consistent set of enzymes is present in gongylidia, including numerous plant biomass-degrading enzymes likely involved in the degradation of polysaccharides, plant toxins, and proteins. Overall, gongylidia contained over three quarters of all biomass-degrading enzymes identified in the L. gongylophorus genome, demonstrating that the majority of the enzymes produced by this fungus for biomass breakdown are ingested by the ants. We also identify a set of 40 of these enzymes enriched in gongylidia compared to whole fungus garden samples, suggesting that certain enzymes may be particularly important in the initial degradation of foliar material. Our work sheds light on the complex interplay between leaf-cutter ants and their fungal symbiont that allows for the host insects to occupy an herbivorous niche by indirectly deriving energy from plant biomass.},
doi = {10.1371/journal.pone.0134752},
journal = {PLoS ONE},
number = 8,
volume = 10,
place = {United States},
year = {Fri Aug 28 00:00:00 EDT 2015},
month = {Fri Aug 28 00:00:00 EDT 2015}
}
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