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

Andrei S. Steindorff, Kyungyong Seong, Akiko Carver, Sara Calhoun, Monika S. Fischer, Kyra Stillman, Haowen Liu, Elodie Drula, Bernard Henrissat, Hunter J. Simpson, Jonathan S. Schilling, Anna Lipzen, Guifen He, Mi Yan, Bill Andreopoulos, Jasmyn Pangilinan, Kurt LaButti, Vivian Ng, Matthew Traxler, Thomas D. BrunsIgor V. Grigoriev

Research output: Contribution to journalArticlepeer-review

6 Scopus citations

Abstract

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 the orders Pezizales and Agaricales, 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 pyrophilous Pezizales fungi isolated after the 2013 Rim Fire near Yosemite Park in California, USA: 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 responses to stress and the 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 fungi fall between those in mesophilic/nonpyrophilous and thermophilic fungi. A comparative transcriptome analysis of P. domesticum under two conditions – growing on charcoal, and during sexual development – identified modules of genes that are co-expressed in the charcoal and light-induced sexual development conditions. In addition, environmental sensors such as transcription factors STE12, LreA, LreB, VosA, and EsdC were upregulated in the charcoal condition. 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.

Original languageEnglish (US)
Pages (from-to)1154-1167
Number of pages14
JournalNew Phytologist
Volume236
Issue number3
DOIs
StatePublished - Nov 2022

Bibliographical note

Funding Information:
We are grateful to Prof. Irina Druzhinina for kindly offering advice on fungal ecology and the structure of the manuscript. The work (project 10.46936/10.25585/60001080) by the US Department of Energy (DOE) Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the US DOE under Contract no. DE‐AC02‐05CH11231. The work was also funded by the Department of Energy grants DE‐SC0016365 to TDB and IVG and DE‐SC0020351 to TDB, MT and IVG.

Publisher Copyright:
© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.

Keywords

  • fungal genomics
  • pyronema
  • pyrophilous fungi
  • sexual development
  • wildfires

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