Wood decay under anoxia by the brown-rot fungus Fomitopsis pinicola
Robert Röllig, Annie Lebreton, Lucia Grenga, Rosalie Cresswell, Signe Lett, Theodora Tryfona, David Navarro, Julien Lambert, Sacha Grisel, Isabelle Gimbert, Helle Juel Martens, Guylaine Miotello, Xiaolan Yu, Élodie Drula, Marie‐Noëlle Rosso, Lionel Tarrago, Bernard Henrissat, Katja S. Johansen, R. Dupree, Jean Armengaud, Paul Dupree, Jean‐Guy Berrin
Abstract
Basidiomycete fungi are the main decomposers of dead wood with an impact on the global carbon cycle. Their degradative mechanisms have been well-studied under aerobic conditions. Here, we study their activity in oxygen-depleted environments. We use metaproteomics in a field study to identify active wood-decomposing fungi and their enzymes at different depths from the wood surface, including in oxygen-depleted conditions. In vitro, we observe that the brown-rot fungus Fomitopsis pinicola can grow on wood in complete anoxia. Using 13C solid-state NMR, we demonstrate the degradation of plant cell-wall polysaccharides and fungal growth in the absence of oxygen. Proteomic analyses reveal that F. pinicola switches from a Fenton chemistry-based process under aerobic conditions to the secretion of plant cell wall-active enzymes in anoxia. Our finding that wood decay fungi can thrive in complete anoxia provides a deeper understanding of lignocellulose degradation mechanisms in nature and raises opportunities for the development of bio-inspired anaerobic processes. The degradation of dead wood by basidiomycete fungi relies on Fenton chemistry under aerobic conditions. Here, Röllig et al. show that these fungi can also thrive and degrade wood in anoxia, switching from a Fenton chemistry-based process to the secretion of plant cell wall-active enzymes.