Wood decay under anoxia by the brown-rot fungus Fomitopsis pinicola

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.