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.

Welcome to the Atta world: A framework for understanding the effects of leaf‐cutter ants on ecosystem functions

“…Fungal gardens are hot spots of enzymatic activity and decomposition. The symbiotic fungus and associated micro‐organisms produce up to 160 biomass‐degrading enzymes including lignocellulases, pectinases, xylanases, amylases and cellulases that decompose a variety of substrates (Aylward et al, ,; Khadempour et al, ). Simple plant substrates, such as starch and pectin, are quickly decomposed near the top of the fungal garden.…”

The good, the bad and the tasty: The many roles of mushrooms

“…2013) and proteomic data (Kooij et al., 2014b, Aylward et al., 2015) has greatly advanced our understanding of the association between L. gongylophorus and the leaf-cutter ants. The genome of L. gongylophorus was recently sequenced from a strain isolated from an Atta cephalotes leaf-cutter ant colony in Gamboa, Panama (Aylward et al.…”

Fungal Genomes and Insights into the Evolution of the Kingdom

“…The "domesticated" fungus cultivated by leaf cutter ants, Leucoagaricus gongylophorus, has an expansion of CAZymes related to polysaccharide degradation. These enzymes are differentially expressed depending on the plant substrates 'fed' to the fungus garden by leaf cutter farming ants [143][144][145][146][147][148][149]. The specialized gongylidia that are swellings of the hyphal tip have evolved to provide a sugar nutrient source for the ants in exchange for the the input of leaf and plant material into the fungal garden.…”

“…The specialized gongylidia that are swellings of the hyphal tip have evolved to provide a sugar nutrient source for the ants in exchange for the the input of leaf and plant material into the fungal garden. The expansion and specialization of the fungal enzyme families necessary for rapid extraction of carbohydrates from plant material has likely been driven by this highly mutualistic symbiosis [147][148][149].…”