Summary 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 a third of all known budding yeast diversity. Here we establish a robust genus-level phylogeny comprised of 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.

Cell-cycle checkpoints and DNA repair processes protect organisms from potentially lethal mutational damage. Compared to other budding yeasts in the subphylum Saccharomycotina, we noticed that a lineage in the genus Hanseniaspora exhibited very high evolutionary rates, low Guanine–Cytosine (GC) content, small genome sizes, and lower gene numbers. To better understand Hanseniaspora evolution, we analyzed 25 genomes, including 11 newly sequenced, representing 18/21 known species in the genus. Our phylogenomic analyses identify two Hanseniaspora lineages, a faster-evolving lineage (FEL), which began diversifying approximately 87 million years ago (mya), and a slower-evolving lineage (SEL), which began diversifying approximately 54 mya. Remarkably, both lineages lost genes associated with the cell cycle and genome integrity, but these losses were greater in the FEL. E.g., all species lost the cell-cycle regulator WHIskey 5 ( WHI5 ), and the FEL lost components of the spindle checkpoint pathway (e.g., Mitotic Arrest-Deficient 1 [ MAD1 ], Mitotic Arrest-Deficient 2 [ MAD2 ]) and DNA-damage–checkpoint pathway (e.g., Mitosis Entry Checkpoint 3 [ MEC3 ], RADiation sensitive 9 [ RAD9 ]). Similarly, both lineages lost genes involved in DNA repair pathways, including the DNA glycosylase gene 3-MethylAdenine DNA Glycosylase 1 ( MAG1 ), which is part of the base-excision repair pathway, and the DNA photolyase gene PHotoreactivation Repair deficient 1 ( PHR1 ), which is involved in pyrimidine dimer repair. Strikingly, the FEL lost 33 additional genes, including polymerases (i.e., POLymerase 4 [ POL4 ] and POL32 ) and telomere-associated genes (e.g., Repressor/activator site binding protein-Interacting Factor 1 [ RIF1 ], Replication Factor A 3 [ RFA3 ], Cell Division Cycle 13 [ CDC13 ], Pbp1p Binding Protein [ PBP2 ]). Echoing these losses, molecular evolutionary analyses reveal that, compared to the SEL, the FEL stem lineage underwent a burst of accelerated evolution, which resulted in greater mutational loads, homopolymer instabilities, and higher fractions of mutations associated with the common endogenously damaged base, 8-oxoguanine. We conclude that Hanseniaspora is an ancient lineage that has diversified and thrived, despite lacking many otherwise highly conserved cell-cycle and genome integrity genes and pathways, and may represent a novel, to our knowledge, system for studying cellular life without them.

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The influence of three commonly used fungicides (iprodione, pyrimethanil and fludioxonil plus cyprodinil) on the density and diversity of yeast populations present on grape berries was evaluated. At the time of harvest, the fungicide residues on grapes were below the maximum permitted levels. In general, larger yeast counts were found on the treated grapes than on the control samples. Among 23 species identified, Cryptococcus magnus, Rhodotorula glutinis and Sporidiobolus pararoseus dominated on sound grape berries. The results showed that the tested fungicides had only a minor impact on the composition of grape berry communities in comparison with the effect of weather conditions and the mode of grape berry sampling. Halo assays using filter discs loaded with fungicides were used as in vitro tests of the sensitivity of grape berry isolates. The fungicide containing pyrimethanil suppressed the growth of all basidiomycetous yeast species, while the sporadically occurring fermentative yeasts were unaffected. Fungicides with fludioxonil plus cyprodinil and iprodione as active substances showed specificity for certain species. Our results suggest that after the safety interval, the presence of fungicides has a minor impact on the composition of grape berry communities, although at the time of fungicide applications, the yeast species composition changes.