The termite fungal cultivar Termitomyces combines diverse enzymes and oxidative reactions for plant biomass conversion

Abstract

Macrotermitine termites have domesticated fungi in the genus Termitomyces as their primary food source using pre-digested plant biomass. To access the full nutritional value of lignin-enriched plant biomass, the termite-fungus symbiosis requires the depolymerization of this complex phenolic polymer. While most previous work suggests that lignocellulose degradation is accomplished predominantly by the fungal cultivar, our current understanding of the underlying biomolecular mechanisms remains rudimentary. Here, we provide conclusive OMICs and activity-based evidence that Termitomyces partially depolymerizes lignocellulose through the combined actions of high-redox potential oxidizing enzymes (laccases, aryl-alcohol oxidases and a manganese peroxidase), the production of extracellular H2O2 and Fenton-based oxidative degradation, which is catalyzed by a newly described 2-methoxybenzoquinone/hydroquinone redox shuttle system and mediated by secreted chelating dicarboxylic acids. In combination, our approaches reveal a comprehensive depiction of how the efficient biomass degradation mechanism in this ancient insect agricultural symbiosis is accomplished through a combination of white- and brown-rot mechanisms. ImportanceFungus-growing termites have perfected the decomposition of recalcitrant plant biomass to access valuable nutrients by engaging in a tripartite symbiosis with complementary contributions from a fungal mutualist and a co-diversified gut microbiome. This complex symbiotic interplay makes them one of the most successful and important decomposers for carbon cycling in Old World ecosystems. To date, most research has focused on the enzymatic contributions of microbial partners to carbohydrate decomposition. Here we provide genomic, transcriptomic and enzymatic evidence that Termitomyces also employs redox mechanisms, including diverse ligninolytic enzymes and a Fenton-based hydroquinone-catalyzed lignin-degradation mechanism, to break down lignin-rich plant material. Insights into these efficient decomposition mechanisms open new sources of efficient ligninolytic agents applicable for energy generation from renewable sources.