title: Leucoagaricus gongylophorus produces diverse enzymes for the degradation of recalcitrant plant polymers in leaf-cutter ant fungus gardens.
abstract: Plants represent a large reservoir of organic carbon comprised primarily 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 gardens composed primarily of Leucoagaricus gongylophorus, a basidiomycetous fungus 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 and metaproteomic tools, we investigate its role in lignocellulose degradation in the gardens of both Atta cephalotes and Acromyrmex echinatior leaf-cutter ants. We show that L. gongylophorus produces a diversity of lignocellulases in ant 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 likely play an important role in lignocellulose degradation. Our study provides a detailed analysis of plant biomass degradation in leaf-cutter ant fungus gardens and insight into the enzymes underlying the symbiosis between these dominant herbivores and their obligate fungal cultivar.
authors.affiliation: Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, USA.
authors.forename: Frank O
authors.initials: FO
authors.lastname: Aylward
authors.forename: Kristin E
authors.initials: KE
authors.lastname: Burnum-Johnson
authors.forename: Susannah G
authors.initials: SG
authors.lastname: Tringe
authors.forename: Clotilde
authors.initials: C
authors.lastname: Teiling
authors.forename: Daniel M
authors.initials: DM
authors.lastname: Tremmel
authors.forename: Joseph A
authors.initials: JA
authors.lastname: Moeller
authors.forename: Jarrod J
authors.initials: JJ
authors.lastname: Scott
authors.forename: Kerrie W
authors.initials: KW
authors.lastname: Barry
authors.forename: Paul D
authors.initials: PD
authors.lastname: Piehowski
authors.forename: Carrie D
authors.initials: CD
authors.lastname: Nicora
authors.forename: Stephanie A
authors.initials: SA
authors.lastname: Malfatti
authors.forename: Matthew E
authors.initials: ME
authors.lastname: Monroe
authors.forename: Samuel O
authors.initials: SO
authors.lastname: Purvine
authors.forename: Lynne A
authors.initials: LA
authors.lastname: Goodwin
authors.forename: Richard D
authors.initials: RD
authors.lastname: Smith
authors.forename: George M
authors.initials: GM
authors.lastname: Weinstock
authors.forename: Nicole M
authors.initials: NM
authors.lastname: Gerardo
authors.forename: Garret
authors.initials: G
authors.lastname: Suen
authors.forename: Mary S
authors.initials: MS
authors.lastname: Lipton
authors.forename: Cameron R
authors.initials: CR
authors.lastname: Currie
mesh_terms: D000363:Agaricales / Q000201:enzymology* / Q000235:genetics; D000595:Amino Acid Sequence; D000818:Animals; D001000:Ants / Q000502:physiology*; D001483:Base Sequence; D044602:Cellulases / Q000235:genetics* / Q000378:metabolism; D016000:Cluster Analysis; D016681:Genome, Fungal / Q000235:genetics*; D060434:Herbivory / Q000502:physiology; D008031:Lignin / Q000378:metabolism; D008969:Molecular Sequence Data; D010176:Panama; D010802:Phylogeny; D010944:Plants / Q000378:metabolism; D040901:Proteomics; D017422:Sequence Analysis, DNA; D017385:Sequence Homology; D013045:Species Specificity; D013559:Symbiosis / Q000502:physiology*
chemical_list: C036909:lignocellulose; D008031:Lignin; D044602:Cellulases