title: The fungal cultivar of leaf-cutter ants produces specific enzymes in response to different plant substrates.
abstract: Herbivores use symbiotic microbes to help derive energy and nutrients from plant material. Leaf-cutter ants are a paradigmatic example, cultivating their mutualistic fungus Leucoagaricus gongylophorus on plant biomass that workers forage from a diverse collection of plant species. Here, we investigate the metabolic flexibility of the ants' fungal cultivar for utilizing different plant biomass. Using feeding experiments and a novel approach in metaproteomics, we examine the enzymatic response of L. gongylophorus to leaves, flowers, oats or a mixture of all three. Across all treatments, our analysis identified and quantified 1766 different fungal proteins, including 161 putative biomass-degrading enzymes. We found significant differences in the protein profiles in the fungus gardens of subcolonies fed different plant substrates. When provided with leaves or flowers, which contain the majority of their energy as recalcitrant plant polymers, the fungus gardens produced more proteins predicted to break down cellulose: endoglucanase, exoglucanase and β-glucosidase. Further, the complete metaproteomes for the leaves and flowers treatments were very similar, while the mixed substrate treatment closely resembled the treatment with oats alone. This indicates that when provided a mixture of plant substrates, fungus gardens preferentially break down the simpler, more digestible substrates. This flexible, substrate-specific enzymatic response of the fungal cultivar allows leaf-cutter ants to derive energy from a wide range of substrates, which likely contributes to their ability to be dominant generalist herbivores.
authors.affiliation: Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, 53706, USA.|Department of Zoology, University of Wisconsin-Madison, Madison, WI, 53706, USA.|Department of Energy Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI, 53706, USA.
authors.forename: Lily
authors.initials: L
authors.lastname: Khadempour
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, 99352, USA.
authors.forename: Kristin E
authors.initials: KE
authors.lastname: Burnum-Johnson
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, 99352, USA.
authors.forename: Erin S
authors.initials: ES
authors.lastname: Baker
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, 99352, USA.
authors.forename: Carrie D
authors.initials: CD
authors.lastname: Nicora
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, 99352, USA.
authors.forename: Bobbie-Jo M
authors.initials: BM
authors.lastname: Webb-Robertson
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, 99352, USA.
authors.forename: Richard A
authors.initials: RA
authors.lastname: White
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, 99352, USA.
authors.forename: Matthew E
authors.initials: ME
authors.lastname: Monroe
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, 99352, USA.
authors.forename: Eric L
authors.initials: EL
authors.lastname: Huang
authors.affiliation: Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, 99352, USA.
authors.forename: Richard D
authors.initials: RD
authors.lastname: Smith
authors.affiliation: Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, 53706, USA.|Department of Energy Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI, 53706, USA.
authors.forename: Cameron R
authors.initials: CR
authors.lastname: Currie
mesh_terms: D000363:Agaricales / Q000201:enzymology*; D000818:Animals; D001000:Ants / Q000382:microbiology*; D035264:Flowers / Q000378:metabolism; D005656:Fungal Proteins / Q000378:metabolism*; D018515:Plant Leaves / Q000378:metabolism; D010944:Plants / Q000378:metabolism*; D040901:Proteomics; D013559:Symbiosis
chemical_list: D005656:Fungal Proteins
keywords: fungi; leaf-cutter ants; metaproteomics; microbial ecology; symbiosis