Tales from the crypt: genome mining from fungarium specimens improves resolution of the mushroom tree of life

The enormity of the breadth and depth of specimens held within the world's biological collections offers unparalleled opportunities to capture genomic data from across the entire range of known biological diversity. Such a task would take many lifetimes to complete if we could rely only on fresh samples. High-throughput sequencing provides a technical solution to the long-term problems of recalcitrant and degraded DNA typical of museum specimens, suggesting that we may be on the verge of a major collections-based revolution. Although the potential is great, the feasibility of using preserved collections for large-scale, taxonomically comprehensive phylogenomic studies remains unknown. In the present study, we demonstrate the continued relevance of fungarium collections in the genomic era by analyzing a genomic dataset composed of 39 genomes representing 26 family-level clades, including 14 newly generated draft genomes derived from short-read shotgun sequencing of preserved specimens, frozen and freeze-dried material, representing most of the known families of Agaricales. We predicted homologues of 210 putative single copy genes in the newly generated draft genome assemblies, of which 208 were used for phylogenetic reconstruction. Our analyses resulted in a robust and, for the first time, fully supported phylogeny of the Agaricales, enabling the recognition of seven suborders and providing a resource for testing hypotheses of the evolution of mushrooms. Our analysis of optimal combinations of ranked genes using an information theory-based method provides guidance on gene selection for future studies, enabling efficient application of high-throughput sequencing techniques toward unlocking the potential of collections-based research in the genomic era.