Uncovering the hidden diversity of litter-decomposition mechanisms in mushroom-forming fungi

Abstract Litter decomposing Agaricales play key role in terrestrial carbon cycling, but little is known about their decomposition mechanisms. We assembled datasets of 42 gene families involved in plant-cell-wall decomposition from seven newly sequenced litter decomposers and 35 other Agaricomycotina members, mostly white-rot and brown-rot species. Using sequence similarity and phylogenetics, we split the families into phylogroups and compared their gene composition across nutritional strategies. Subsequently, we used Raman spectroscopy to examine the ability of litter decomposers, white-rot fungi, and brown-rot fungi to decompose crystalline cellulose. Both litter decomposers and white-rot fungi share the enzymatic cellulose decomposition, whereas brown-rot fungi possess a distinct mechanism that disrupts cellulose crystallinity. However, litter decomposers and white-rot fungi differ with respect to hemicellulose and lignin degradation phylogroups, suggesting adaptation of the former group to the litter environment. Litter decomposers show high phylogroup diversity, which is indicative of high functional versatility within the group, whereas a set of white-rot species shows adaptation to bulk-wood decomposition. In both groups, we detected species that have unique characteristics associated with hitherto unknown adaptations to diverse wood and litter substrates. Our results suggest that the terms white-rot fungi and litter decomposers mask a much larger functional diversity.