Deciphering taxon-specific metabolic shifts during pathogenic fungal infection in leaf-cutter ant fungal gardens.

Abstract

Leaf-cutter ant fungal gardens are a living library of bioeconomy solutions, where the mutualist fungus Leucoagaricus gongylophorus drives lignocellulose degradation and conversion into valuable bioproducts. However, these gardens are vulnerable to infection by the specialized pathogen Escovopsis weberi, which disrupts garden stability. Despite their ecological importance, the metabolic mechanisms underlying fungal-fungal competition and community-level responses to infection remain poorly understood. To address this gap, we experimentally infected six fungal garden consortia with E. weberi, establishing an infection gradient within each consortium, which we then systematically analyzed using a multi-omics approach. Metabolomic profiling revealed infection-induced alterations in metabolite abundance, while metaproteomic analysis identified fungal-specific shifts in protein levels across a spatiotemporal scale. The integration of multi-omics datasets across all fungal garden consortia provided a comprehensive view of the underlying pathways, revealing that the pathogenic fungus exploits nutrient supplies derived from lignocellulose degradation by native fungi. Reconstruction of active pathways enabled us to trace nutrient flow and map taxon-specific metabolic shifts in response to infection. Specifically, a distinct switch from lysine synthesis by native fungi to lysine catabolism orchestrated by pathogenic fungi. These findings offer a system-level perspective of the molecular alterations driving competitive interactions between native and pathogenic species within the fungal garden consortium. This study not only highlights the power of multi-omics approaches in unraveling the complexity of microbial consortia across ecological scales but also provides an integrated road map to efficiently harness microbiome data for deeper insights into microbial interactions and community responses to perturbations.