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.
Bibliographical noteFunding Information:
We thank the University of Minnesota, the Fulbright Commission, and the Colombian Ministry of Science, Technology, and Innovation for funding to J.D.C. We gratefully acknowledge funding support from U.S. Department of Energy, Biological and Environmental Research program grants DE-SC0019427 and DE-SC0012742 and user facility award EUP50799, each awarded to J.S.S. as the principal investigator. Also, a portion of this research was performed on a project award (10.46936/reso.proj.2019.50461/ 60000058) from the Environmental Molecular Sciences Laboratory, a DOE Office of Science User Facility sponsored by the Biological and Environmental Research program under contract no. DE-AC05-76RL01830.
The LiX beamline is part of the Center for BioMolecular Structure (CBMS), which is primarily supported by the National Institutes of Health, National Institute of General Medical Sciences (NIGMS) through a P30 Grant (P30GM133893), and by the DOE Office of Biological and Environmental Research (KP1605010). LiX also received additional support from NIH Grant S10 OD012331. As part of NSLS-II, a national user facility, work performed at the CBMS is supported in part by the U.S. Department of Energy, Office of Science Basic Energy Sciences Program under contract number DE-SC0012704.
© 2022 Castaño et al.
- Secondary metabolites
- antioxidant activity
- brown rot fungi
- solid state culture
- white rot fungi
- wood decay
PubMed: MeSH publication types
- Journal Article
- Research Support, Non-U.S. Gov't
- Research Support, U.S. Gov't, Non-P.H.S.
- Research Support, N.I.H., Extramural