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.
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 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.
authors: Department of Bacteriology, University of Wisconson-Madison, Madison, Wisconsin, United States of America; Great Lakes Bioenergy Research Center, University of Wisconsin, Madison, Wisconsin, United States of America.
authors: Frank O
authors: FO
authors: Aylward
authors: Department of Bacteriology, University of Wisconson-Madison, Madison, Wisconsin, United States of America; Great Lakes Bioenergy Research Center, University of Wisconsin, Madison, Wisconsin, United States of America.
authors: Lily
authors: L
authors: Khadempour
authors: Department of Bacteriology, University of Wisconson-Madison, Madison, Wisconsin, United States of America; Great Lakes Bioenergy Research Center, University of Wisconsin, Madison, Wisconsin, United States of America.
authors: Daniel M
authors: DM
authors: Tremmel
authors: Department of Bacteriology, University of Wisconson-Madison, Madison, Wisconsin, United States of America; Great Lakes Bioenergy Research Center, University of Wisconsin, Madison, Wisconsin, United States of America.
authors: Bradon R
authors: BR
authors: McDonald
authors: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors: Carrie D
authors: CD
authors: Nicora
authors: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors: Si
authors: S
authors: Wu
authors: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors: Ronald J
authors: RJ
authors: Moore
authors: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors: Daniel J
authors: DJ
authors: Orton
authors: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors: Matthew E
authors: ME
authors: Monroe
authors: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors: Paul D
authors: PD
authors: Piehowski
authors: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors: Samuel O
authors: SO
authors: Purvine
authors: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors: Richard D
authors: RD
authors: Smith
authors: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors: Mary S
authors: MS
authors: Lipton
authors: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America.
authors: Kristin E
authors: KE
authors: Burnum-Johnson
authors: Department of Bacteriology, University of Wisconson-Madison, Madison, Wisconsin, United States of America; Great Lakes Bioenergy Research Center, University of Wisconsin, Madison, Wisconsin, United States of America.
authors: Cameron R
authors: CR
authors: Currie
mesh_terms: D000363:Agaricales / Q000201:enzymology* / Q000502:physiology; D000818:Animals; D001000:Ants / Q000382:microbiology* / Q000502:physiology; D018533:Biomass; D005656:Fungal Proteins / Q000378:metabolism*; D060434:Herbivory / Q000502:physiology*; D025301:Hyphae / Q000201:enzymology / Q000502:physiology; D040901:Proteomics / Q000379:methods; D013559:Symbiosis
chemical_list: D005656:Fungal Proteins