Mitochondria retain their own genome, a hallmark of their bacterial ancestry. Mitochondrial genomes (mtDNA) are highly diverse in size, shape, and structure, despite their conserved function across most eukaryotes. Exploring extreme cases of mtDNA architecture can yield important information on fundamental aspects of genome biology. We discovered that the mitochondrial genomes of a basidiomycete fungus (Termitomyces spp.) contain an inverted repeat (IR), a duplicated region half the size of the complete genome. In addition, we found an abundance of sequences capable of forming G-quadruplexes (G4DNA); structures that can disrupt the double helical formation of DNA. G4DNA is implicated in replication fork stalling, double-stranded breaks, altered gene expression, recombination, and other effects. To determine whether this occurrence of IR and G4DNA was correlated within the genus Termitomyces, we reconstructed the mitochondrial genomes of 11 additional species including representatives of several closely related genera. We show that the mtDNA of all sampled species of Termitomyces and its sister group, represented by the species Tephrocybe rancida and Blastosporella zonata, are characterized by a large IR and enrichment of G4DNA. To determine whether high mitochondrial G4DNA content is common in fungi, we conducted the first broad survey of G4DNA content in fungal mtDNA, revealing it to be a highly variable trait. The results of this study provide important direction for future research on the function and evolution of G4DNA and organellar IRs.

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Ancestral predisposition toward a domesticated lifestyle in the termite-cultivated fungus Termitomyces Highlights d Insect-fecal associations predate the domestication of Termitomyces fungi d A set of morphological traits predisposed lyophylloid fungi toward domestication d Insect-associated lyophylloid fungi have reduced plantdegrading capabilities d This symbiosis may have been facilitated by pre-adaptation of both partners

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A new species of Termitomyces symbiotic with the termite Macrotermes natalensis is described from Africa. As there are no records of field collected basidiocarps within this lineage, traditional basidiocarp-based morphological taxonomy is not practical. While basidiocarps may be obtained rarely from incubation of fungal comb fragments, their practical use for taxonomical purposes is limited. Therefore, the species is described based on an ITS nucleotide sequence, with comparisons to an asexual culture. Based on samples with similar ITS sequences, this species is likely associated with multiple termite hosts across a large part of Africa.