Genome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota

Abstract

Ascomycota, the largest and most well-studied phylum of fungi, contains three subphyla: Saccharomycotina (budding yeasts), Pezizomycotina (filamentous fungi), and Taphrinomycotina (fission yeasts). Despite its importance, we lack a comprehensive genome-scale phylogeny or understanding of the similarities and differences in the mode of genome evolution within this phylum. By examining 1107 genomes from Saccharomycotina (332), Pezizomycotina (761), and Taphrinomycotina (14) species, we inferred a robust genome-wide phylogeny that resolves several contentious relationships and estimated that the Ascomycota last common ancestor likely originated in the Ediacaran period. Comparisons of genomic properties revealed that Saccharomycotina and Pezizomycotina differ greatly in their genome properties and enabled inference of the direction of evolutionary change. The Saccharomycotina typically have smaller genomes, lower guanine-cytosine contents, lower numbers of genes, and higher rates of molecular sequence evolution compared with Pezizomycotina. These results provide a robust evolutionary framework for understanding the diversity and ecological lifestyles of the largest fungal phylum.

Genomic insights into the host specific adaptation of the Pneumocystis genus

“…2c; Supplementary Fig. 1), with a separation of Pneumocystis and Schizosaccharomyces genera around 512 mya (CI: 822-203 mya), which is consistent with independent estimates of the origin of Taphrinomycota crown group at 530 mya 21 . The Pneumocystis genus thereafter divided into two main clades, P1 consisting of P. jirovecii, P. macacae, P. oryctolagi, and P. canis, and P2 consisting of species infecting rodents (P. carinii, P. wakefieldiae, and P. murina) (Fig.…”

Examination of gene loss in the DNA mismatch repair pathway and its mutational consequences in a fungal phylum

“…Branches are colored by subphylum; budding yeasts / Saccharomycotina (n = 332 species) are in red, fission yeasts / Taphrinomycotina (n = 14 species) are in purple, and filamentous fungi / Pezizomycotina (n = 761 species) are in green. Taxon names have been omitted from the phylogeny for visualization purposes; the phylogenetic tree with taxon names can be found in Figure S1 and Shen et al (2020). The inset phylogenetic tree shows the HLT (in blue) and LLT (in black), with the blue box beneath highlighting them.…”

“…Although DNA repair genes are generally highly conserved, certain fungal lineages have been reported to have a more limited repertoire of DNA repair genes, particularly within the phylum Ascomycota. For example, budding yeasts (subphylum Saccharomycotina) and fission yeasts (Taphrinomycotina) have fewer DNA repair genes than filamentous fungi (Pezizomycotina) (Milo et al 2019;Shen et al 2020). Furthermore, DNA repair genes that were lost from budding yeasts and fission yeasts are more likely to also be lost in filamentous fungi (Milo et al 2019).…”

Novakomyces olei sp. nov., the First Member of a Novel Taphrinomycotina Lineage

“…According to single locus or multigene phylogenetic analyses, the fungi assigned to Taphrinomycotina form either mono- or paraphyletic groups depending on the taxon sampling, the analysed phylogenetic markers, and the applied algorithm [ 3 ]. However, phylogenomic analyses support the monophyly of the taxa of Taphrinomycotina involved in the analyses (e.g., [ 8 , 9 , 10 , 11 , 12 ]).…”