Leucoagaricus gongylophorus Produces Diverse Enzymes for the Degradation of Recalcitrant Plant Polymers in Leaf-Cutter Ant Fungus Gardens

Journal Article · Wed Jun 12 00:00:00 EDT 2013 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/AEM.03833-12· OSTI ID:1088602

Aylward, Frank O. ^[1]; Burnum-Johnson, Kristin E. ^[2]; Tringe, Susannah G. ^[3]; Teiling, Clotilde ^[4]; Tremmel, Daniel ^[5]; Moeller, Joseph ^[1]; Scott, Jarrod J. ^[1]; Barry, Kerrie W. ^[3]; Piehowski, Paul D. ^[2]; Nicora, Carrie D. ^[2]; Malfatti, Stephanie ^[3]; Monroe, Matthew E. ^[2]; Purvine, Samuel O. ^[2]; Goodwin, Lynne A. ^[3]; Smith, Richard D. ^[2]; Weinstock, George ^[6]; Gerardo, Nicole ^[7]; Suen, Garret ^[3]; Lipton, Mary S. ^[2]; Currie, Cameron R. ^[8]

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1. Univ. of Wisconsin, Madison, WI (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
3. Dept. of Energy Joint Genome Inst., Walnut Creek, CA (United States)
4. Roche Diagnostics, Indianapolis, IN (United States)
5. Univ. of Wisconsin, Madison, WI (United States)
6. Washington Univ. School of Medicine, St. Louis, MS (United States)
7. Emory Univ., Atlanta, GA (United States)
8. Univ. of Wisconsin, Madison, WI (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Smothsonian Tropical Research Inst., Balboa (Panama)

Plants represent a large reservoir of organic carbon comprised largely of recalcitrant polymers that most metazoans are unable to deconstruct. Many herbivores gain access to nutrients in this material indirectly by associating with microbial symbionts, and leaf-cutter ants are a paradigmatic example. These ants use fresh foliar biomass as manure to cultivate fungus gardens composed primarily of Leucoagaricus gongylophorus, a basidiomycetous symbiont that produces specialized hyphal swellings that serve as a food source for the host ant colony. Although leaf-cutter ants are conspicuous herbivores that contribute substantially to carbon turnover in Neotropical ecosystems, the process through which plant biomass is degraded in their fungus gardens is not well understood. Here we present the first draft genome of L. gongylophorus, and using genomic, metaproteomic, and phylogenetic tools we investigate its role in lignocellulose degradation in the fungus gardens of both Atta cephalotes and Acromyrmex echinatior leaf-cutter ants. We show that L. gongylophorus produces a diversity of lignocellulases in fungus gardens, and is likely the primary driver of plant biomass degradation in these ecosystems. We also show that this fungus produces distinct sets of lignocellulases throughout the different stages of biomass degradation, including numerous cellulases and laccases that may be playing an important but previously uncharacterized role in lignocellulose degradation. Our study provides a comprehensive analysis of plant biomass degradation in leaf-cutter ant fungus gardens and provides insight into the molecular dynamics underlying the symbiosis between these dominant herbivores and their obligate fungal cultivar.

• Research Organization: Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
• Sponsoring Organization: USDOE
• DOE Contract Number: AC05-76RL01830
• OSTI ID: 1088602
• Report Number(s): PNNL-SA-92750; 47418; KP1601010
• Journal Information: Applied and Environmental Microbiology, Vol. 79, Issue 12; ISSN 0099-2240
• Publisher: American Society for Microbiology
• Country of Publication: United States
• Language: English

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Environmental Molecular Sciences Laboratory