Genome reduction and relaxed selection is associated with the transition to symbiosis in the basidiomycete genus Podaxis
Benjamin H. Conlon,
Cene Gostinčar,
Janis Fricke,
Nina B. Kreuzenbeck,
Jan-Martin Daniel,
Malte S.L. Schlosser,
Nils Peereboom,
Duur K. Aanen,
Z. Wilhelm de Beer,
Christine Beemelmanns,
Nina Gunde-Cimerman,
Michael Poulsen
Affiliations
Benjamin H. Conlon
Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen Ø, Denmark; Corresponding author
Cene Gostinčar
Department of Biology, Biotechnical Faculty, University of Ljubljana, 1000 Ljubljana, Slovenia
Janis Fricke
Leibniz Institute for Natural Product Research and Infection Biology, Hans-Knoll-Institute, Chemical Biology, 07745 Jena, Germany
Nina B. Kreuzenbeck
Leibniz Institute for Natural Product Research and Infection Biology, Hans-Knoll-Institute, Chemical Biology, 07745 Jena, Germany
Jan-Martin Daniel
Leibniz Institute for Natural Product Research and Infection Biology, Hans-Knoll-Institute, Chemical Biology, 07745 Jena, Germany
Malte S.L. Schlosser
Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen Ø, Denmark
Nils Peereboom
Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen Ø, Denmark
Duur K. Aanen
Department of Plant Sciences, Laboratory of Genetics, Wageningen University, 6708 PB Wageningen, the Netherlands
Z. Wilhelm de Beer
Department of Biochemistry, Genetics, and Microbiology, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria 0002, South Africa
Christine Beemelmanns
Leibniz Institute for Natural Product Research and Infection Biology, Hans-Knoll-Institute, Chemical Biology, 07745 Jena, Germany
Nina Gunde-Cimerman
Department of Biology, Biotechnical Faculty, University of Ljubljana, 1000 Ljubljana, Slovenia
Michael Poulsen
Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen Ø, Denmark; Corresponding author
Summary: 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.