Genome reduction and relaxed selection is associated with the transition to symbiosis in the basidiomycete genus Podaxis

Insights into the genomic consequences of symbiosis for basidiomycete fungi associated with social insects remain sparse. Capitalizing on viability of spores from centuries-old herbarium specimens of free-living, facultative, and specialist termite-associated Podaxis fungi, we obtained genomes of 10 specimens, including two type species described by Linnaeus >240 years ago. We document that the transition to termite association was accompanied by significant reductions in genome size and gene content, accelerated evolution in protein-coding genes, and reduced functional capacities for oxidative stress responses and lignin degradation. Functional testing confirmed that termite specialists perform worse under oxidative stress, while all lineages retained some capacity to cleave lignin. Mitochondrial genomes of termite associates were significantly larger; possibly driven by smaller population sizes or reduced competition, supported by apparent loss of certain biosynthetic gene clusters. Our findings point to relaxed selection that mirrors genome traits observed among obligate endosymbiotic bacteria of many insects.SUPPLEMENTARY MATERIAL: DOCUMENT S1. Figures S1–S10 and Tables S1, S2, S3, and S8TABLE S4. Orthogroups which were present in at least two genomes with the lifestyles in which they were found, related to Figure 2BTABLE S5. Predicted CAZymes, EC numbers and substrates from HotPep analysis, related to Figures 3A–3ETABLE S6. Functionally-enriched GO terms based on dcGO with an adjusted p-value cutoff of padj = 0.05, related to Figure 2BTABLE S7. Growth measurements for Podaxis strains grown on YMEA enriched with 0, 5 and 20 mM H2O2, related to Figure 3FThe Danish Council for Independent Research, the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) and the Slovenian Research Agency.https://www.cell.com/iscience/homehj2021BiochemistryForestry and Agricultural Biotechnology Institute (FABI)GeneticsMicrobiology and Plant Patholog