Genomic and Experimental Investigations of Auriscalpium and Strobilurus Fungi Reveal New Insights into Pinecone Decomposition

Saprophytic fungi play vital roles in nutrient cycling and ecosystem dynamics. However, our understanding of how saprophytic fungi interact with each other to decompose organic matter is very limited. Here, we conducted field surveys of pinecone-colonizing/decomposing mushrooms, investigated the chemical compositions of decomposing pinecones, and analyzed seven new genomes of three pairs of mushrooms in the genera Auriscalpium and Strobilurus with substrate specificities. Each pair of mushrooms successively colonizes the pinecones of a different pine species: A. orientale-S. luchuensis on Pinus yunnanensis, A. vulgare-S. stephanocystis on Pinus sylvestris, and A. microsporum-S. pachcystidiatus/S. orientalis on Pinus armandii. Our analyses revealed evidence for both competition and cooperation between Auriscalpium and Strobilurus fungi during pinecone decomposition. Their successive colonization of the two fungi groups with complementary profiles of carbohydrate-active enzymes enabled efficient decomposition and utilization of pinecones. The Auriscalpium fungi are highly effective at utilizing the recalcitrant primary organic carbons such as lignin and hemicellulose in freshly fallen pinecones. The decomposition by Auriscalpium fungi enabled the successive colonization by Strobilurus fungi which can produce an arsenal of secondary metabolites such as strobilurins to inhibit other fungi and have abundant carbohydrate-active enzymes for effective utilization of the remaining organic compounds in pinecones.