TY - JOUR

T1 - Genome reduction and relaxed selection is associated with the transition to symbiosis in the basidiomycete genus Podaxis

AU - Conlon, Benjamin H.

AU - Gostinčar, Cene

AU - Fricke, Janis

AU - Kreuzenbeck, Nina B.

AU - Daniel, Jan-Martin

AU - Schlosser, Malte S. L.

AU - Peereboom, Nils

AU - Aanen, Duur K.

AU - de Beer, Z. Wilhelm

AU - Beemelmanns, Christine

AU - Gunde-Cimerman, Nina

AU - Poulsen, Michael

N1 - Funding Information: We would like to thank Riana Jacobs at the South African Agricultural Research Council; Henning Knudsen at The Natural History Museum of Denmark; Paul F?rster and Michael Mathieson at the Queensland Herbarium in Australia; the Linnaean Society of London and Bryn Dentinger for access to specimens; Christian Lange for assisting with the herbarium loans; Isabelle Charmantier for photos of the type specimen; Sylvia Mathiasen for laboratory assistance; and Pepijn Kooij, Robert Murphy, and Lucie Bergeron for bioinformatics suggestions. This work was funded by The Danish Council for Independent Research (DFF - 7014-00178) to M.P. and the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany's Excellence Strategy ? EXC 2051 ? Project-ID 390713860 to C.B. and J.F.; N.G.-C. and C.G. acknowledge the financial support from the state budget of the Slovenian Research Agency (Research Project J4-2549, Research Programmes P1-0198 and P1-0170, Infrastructural Center Mycosmo). The study was conceived by B.H.C. D.K.A. Z.W.d.B. C.B. N.G.-C. and M.P. the laboratory work was performed by B.H.C. J.-M.D. M.S.L.S. and N.P. bioinformatic analyses were performed by B.H.C. C.G. J.F. N.B.K. and N.P. the first manuscript draft was written by B.H.C. with input from all authors, and all authors have read and approved the final version of the manuscript. The authors declare no competing interests. One or more of the authors of this paper self-identifies as a member of the LGBTQ+ community. The author list of this paper includes contributors from the location where the research was conducted who participated in the data collection, design, analysis, and/or interpretation of this work. Funding Information: We would like to thank Riana Jacobs at the South African Agricultural Research Council; Henning Knudsen at The Natural History Museum of Denmark; Paul Förster and Michael Mathieson at the Queensland Herbarium in Australia; the Linnaean Society of London and Bryn Dentinger for access to specimens; Christian Lange for assisting with the herbarium loans; Isabelle Charmantier for photos of the type specimen; Sylvia Mathiasen for laboratory assistance; and Pepijn Kooij, Robert Murphy, and Lucie Bergeron for bioinformatics suggestions. This work was funded by The Danish Council for Independent Research (DFF - 7014-00178 ) to M.P. and the Deutsche Forschungsgemeinschaft ( DFG , German Research Foundation) under Germany's Excellence Strategy – EXC 2051 – Project-ID 390713860 to C.B. and J.F.; N.G.-C. and C.G. acknowledge the financial support from the state budget of the Slovenian Research Agency (Research Project J4-2549 , Research Programmes P1-0198 and P1-0170, Infrastructural Center Mycosmo). Publisher Copyright: © 2021 The Author(s)

PY - 2021

Y1 - 2021

N2 - 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.

AB - 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.

KW - Biological sciences

KW - Genetics

KW - genomics

U2 - 10.1016/j.isci.2021.102680

DO - 10.1016/j.isci.2021.102680

M3 - Journal article

C2 - 34189441

AN - SCOPUS:85107928601

VL - 24

JO - iScience

JF - iScience

SN - 2589-0042

IS - 6

M1 - 102680

ER -