The fungus gardens of leaf-cutter ants undergo a distinct physiological transition during biomass degradation

Leaf-cutter ants are dominant herbivores in ecosystems throughout the Neotropics that feed on fungus gardens cultivated on fresh foliar biomass. Although recent investigations have shed light on how plant biomass is degraded in fungus gardens, the cycling of nutrients that takes place in these specialized microbial ecosystems is still not well understood. Here, using metabolomic and metaproteomic techniques, we examine the dynamics of nutrient turnover in these gardens. Our results reveal that numerous free amino acids and sugars are depleted throughout the process of biomass degradation, indicating that easily accessible nutrients from plant material are readily consumed by microbes in these ecosystems. Accumulation of cellobiose and lignin derivatives near the end of the degradation process is consistent with previous characterization of lignocellulases produced by the fungal cultivar of the ants. Our results also suggest that ureides may be an important source of nitrogen in fungus gardens, especially during nitrogen-limiting conditions. No free arginine was detected in our metabolomic experiments despite evidence that the host ants cannot produce this amino acid, suggesting that biosynthesis of this metabolite may be tightly regulated in fungus gardens. These results provide new insights into microbial community-level processes that underlie this important ant-fungus symbiosis.