Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum

• Published in: Cell 2018-11, Vol.175 (6), p.1533-1545.e20
• Main Authors: Shen, Xing-Xing, Opulente, Dana A., Kominek, Jacek, Zhou, Xiaofan, Steenwyk, Jacob L., Buh, Kelly V., Haase, Max A.B., Wisecaver, Jennifer H., Wang, Mingshuang, Doering, Drew T., Boudouris, James T., Schneider, Rachel M., Langdon, Quinn K., Ohkuma, Moriya, Endoh, Rikiya, Takashima, Masako, Manabe, Ri-ichiroh, Čadež, Neža, Libkind, Diego, Rosa, Carlos A., DeVirgilio, Jeremy, Hulfachor, Amanda Beth, Groenewald, Marizeth, Kurtzman, Cletus P., Hittinger, Chris Todd, Rokas, Antonis
• Format: Article
• Language: English
• Subjects: and reductive evolution; Ascomycota; BASIC BIOLOGICAL SCIENCES; genomics; high-throughput sequencing; horizontal gene transfer; metabolic traits; molecular dating; phylogenetics; phylogenomics; Saccharomycotina
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2018.10.023

Budding yeasts (subphylum Saccharomycotina) are found in every biome and are as genetically diverse as plants or animals. To understand budding yeast evolution, we analyzed the genomes of 332 yeast species, including 220 newly sequenced ones, which represent nearly one-third of all known budding yeast diversity. Here, we establish a robust genus-level phylogeny comprising 12 major clades, infer the timescale of diversification from the Devonian period to the present, quantify horizontal gene transfer (HGT), and reconstruct the evolution of 45 metabolic traits and the metabolic toolkit of the budding yeast common ancestor (BYCA). We infer that BYCA was metabolically complex and chronicle the tempo and mode of genomic and phenotypic evolution across the subphylum, which is characterized by very low HGT levels and widespread losses of traits and the genes that control them. More generally, our results argue that reductive evolution is a major mode of evolutionary diversification. [Display omitted] •332 genomes, including 220 newly sequenced, covering ∼1/3 of known budding yeasts•Genome-scale inference of robust phylogeny and time tree of budding yeast subphylum•Reconstruction of 45 metabolic traits infers complex budding yeast common ancestor•Reductive evolution of traits and genes is a major mode of evolutionary diversification An integrated phylogeny of over 300 budding yeast species encompasses the natural diversity and history of diversification of Saccharomycotina with insights into a metabolically complex common ancestor and common reductive evolution leading to metabolic specialization.