Diversity of genomic adaptations to post-fire environment in Pezizales fungi points to a crosstalk between charcoal tolerance and sexual development.

Wildfires drastically impact the soil environment altering the soil organic matter, forming pyrolyzed compounds, and markedly reducing the diversity of microorganisms. Pyrophilous fungi, especially the species from Pezizales and Agaricales orders, are fire-responsive fungal colonizers of post-fire soil that have historically been found fruiting on burned soil and thus may encode mechanisms of processing these compounds in their genomes.Pyrophilous fungi are diverse. In this work, we explored this diversity and sequenced six new genomes of Pezizales pyrophilous fungi isolated after the 2013 Rim fire near Yosemite Park in California, United States: Pyronema domesticum, Pyronema omphalodes, Tricharina praecox, Geopyxis carbonaria, Morchella snyderi, and Peziza echinospora.A comparative genomics analysis revealed the enrichment of gene families involved in response to stress and degradation of pyrolyzed organic matter. In addition, we found that both protein sequence lengths and G+C content in the third base of codons (GC3) in pyrophilous fungiare those in mesophilic/non-pyrophilous and thermophilic fungi.A comparative transcriptome analysis of P. domesticum growing on charcoal and during sexual developmental stages identified modules of genes co-expressed in charcoal and light-induced sexual development. In addition, environmental sensors such as transcription factors STE12, LreA, LreB, VosA, and EsdC were up-regulated in charcoal.Taken together, these results highlight genomic adaptations of pyrophilous fungi and indicate a potential connection between charcoal tolerance and fruiting body formation in P. domesticum.