Pan-omic characterization of plant polymer degradation in leaf-cutter ant fungus gardens

Leaf-cutter ants are hallmark examples of insect herbivores that gain access to nutrients in plant material through symbioses with microbes.  Through the cultivation of fungus-bacterium “gardens” on fresh foliar material, these ants are able to access nutrients in plant biomass that would otherwise be unavailable.  Here using proteomic and metabolomic analyses we investigate lignocellulose degradation in the gardens of laboratory-kept 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 while the bacterial community plays a dominate role in nutrient cycling by converting this nitrogen-poor forage into B-vitamins, amino acids and other cellular components.  We show that the fungus produces distinct sets of lignocellulases throughout the different stages of biomass degradation; many cellulases that likely play an important role in lignocellulose degradation localize to the bottom strata which also shows an accumulation of cellobiose and lignin derivative metabolites.  Using proteomic measurements we investigate changes in lignocellulose expression due to substrate availability in Atta cephalotes colonies fed leaves, flowers, oats or a mix of all three.  In these analyses we show that the fungal cultivar produces enzymes to break crystalline cellulose when lignocellulose rich food sources, such as leaves and flowers are available.  These discoveries provide new enzyme targets that could be tested for their biochemical properties and application in bioethanol production.