Proteomics reveals synergy in biomass conversion between fungal enzymes and inorganic Fenton chemistry in leaf-cutting ant colonies

The herbivorous symbiosis between leaf-cutting ants and fungal cultivars processes biomass via ant fecal fluid mixed with munched plant substrate before fungal degradation. Here we present a full proteome of the fecal fluid of Acromyrmex leaf-cutting ants, showing that most proteins function as biomass degrading enzymes and that ca. 80% are produced by the fungal cultivar and ingested, but not digested, by the ants. Hydrogen peroxide producing oxidoreductases were remarkably common in the fecal proteome, inspiring us to test a scenario in which hydrogen peroxide reacts with iron in the fecal fluid to form reactive oxygen radicals after which oxidized iron is reduced by other fecal-fluid enzymes. Our biochemical assays confirmed that these cyclical Fenton reactions do indeed take place in special substrate pellets, presumably to degrade recalcitrant lignocellulose. This implies that the symbiosis manages a combination of chemical and enzymatic degradation, an achievement that surpasses current human bioconversion technology.