Metabolomics Highlights Different Life History Strategies of White and Brown Rot Wood-Degrading Fungi

ABSTRACT White and brown rot fungi efficiently deconstruct lignocellulose in wood, Earth’s largest pool of aboveground biotic carbon and an important natural resource. Despite its vital importance, little is known about the metabolomic signatures among fungal species and nutritional modes (rot types). In this study, we used GC-MS metabolomics in solid wood substrates (in planta) to compare brown rot fungi (Rhodonia placenta and Gloeophylum trabeum) and white rot fungi (Trametes versicolor and Pleurotus ostreatus) at two decay stages (earlier and later), finding identifiable patterns for brown rot fungi at later decay stages. These patterns occurred in highly reducing environments that were not observed in white rot fungi. Metabolomes measured among the two white rot fungi were notably different, but we found a potential biomarker compound, galactitol, that was characteristic to white rot taxa. In addition, we found that white rot fungi were more efficient at catabolizing phenolic compounds that were originally present in wood. Collectively, white rot fungi were characterized by measured sugar release relative to higher carbohydrate solubilization by brown rot fungi, a distinction in soluble sugar availability that might shape success in the face of “cheater” competitors. This need to protect excess free sugars may explain the differentially high brown rot fungal production of pyranones and furanones, likely linked to an expansion of polyketide synthase genes. IMPORTANCE Despite the ecological and economic importance of wood-degrading fungi, little is known about the array of metabolites that fungi produce during wood decomposition. This study provides an in-depth insight into the wood decomposition process by analyzing and comparing the changes of >100 compounds produced by fungi with metabolic distinct nutritional modes (white and brown rot fungi) at different decay stages. We found a unique pattern of metabolites that correlated well with brown rot (carbohydrate selective mode) in later decay. These compounds were in line with some of the physiochemical and genetic features previously seen in these fungi such as a faster sugar release, lower pH, and the expansion of polyketide-synthase genes compared to white rot fungi (lignin-degrading mode). This study provides spatiotemporally resolved mechanism insights as well as critical groundwork that will be valuable for studies in basic biology and ecology, as well as applied biomass deconstruction and bioremediation.