Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts

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.Fil: Steenwyk, Jacob L.. Vanderbilt University; Estados UnidosFil: Opulente, Dana A.. University of Wisconsin; Estados UnidosFil: Kominek, Jacek. University of Wisconsin; Estados UnidosFil: Shen, Xing-Xing. Vanderbilt University; Estados UnidosFil: Zhou, Xiaofan. South China Agricultural University; ChinaFil: Labella, Abigail L.. Vanderbilt University; Estados UnidosFil: Bradley, Noah P.. Vanderbilt University; Estados UnidosFil: Eichman, Brandt F.. Vanderbilt University; Estados UnidosFil: Cadez, Neza. University of Ljubljana; EsloveniaFil: Libkind Frati, Diego. Universidad Nacional del Comahue. Centro Regional Universitario Bariloche; ArgentinaFil: DeVirgilio, Jeremy. United States Department of Agriculture. Agricultural Research Service; ArgentinaFil: Hulfachor, Amanda Beth. University of Wisconsin; Estados UnidosFil: Kurtzman, Cletus P.. United States Department of Agriculture. Agricultural Research Service; ArgentinaFil: Hittinger, Chris Todd. University of Wisconsin; Estados UnidosFil: Rokas, Antonis. Vanderbilt University; Estados Unido

Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum

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.Fil: Shen, Xing-Xing. Vanderbilt University; Estados UnidosFil: Opulente, Dana A.. University of Wisconsin; Estados UnidosFil: Kominek, Jacek. University of Wisconsin; Estados UnidosFil: Zhou, Xiaofan. Vanderbilt University; Estados Unidos. South China Agricultural University; ChinaFil: Steenwyk, Jacob L.. Vanderbilt University; Estados UnidosFil: Buh, Kelly V.. University of Wisconsin; Estados UnidosFil: Haase, Max A.B.. University of Wisconsin; Estados Unidos. University of New York. School of Medicine; Estados UnidosFil: Wisecaver, Jennifer H.. Purdue University; Estados Unidos. Vanderbilt University; Estados UnidosFil: Wang, Mingshuang. Vanderbilt University; Estados UnidosFil: Doering, Drew T.. University of Wisconsin; Estados UnidosFil: Boudouris, James T.. University of Wisconsin; Estados UnidosFil: Schneider, Rachel M.. University of Wisconsin; Estados UnidosFil: Langdon, Quinn K.. University of Wisconsin; Estados UnidosFil: Ohkuma, Moriya. Riken BioResource Research Center. Japan Collection of Microorganisms; JapónFil: Endoh, Rikiya. Riken BioResource Research Center. Japan Collection of Microorganisms; JapónFil: Takashima, Masako. Riken BioResource Research Center. Japan Collection of Microorganisms; JapónFil: Manabe, Ri-ichiroh. Riken Center for Integrative Medical Sciences; Japón. Riken Center For Life Science Technologies; JapónFil: Čadež, Neža. University of Ljubljana; EsloveniaFil: Libkind Frati, Diego. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto Andino Patagónico de Tecnologías Biológicas y Geoambientales. Universidad Nacional del Comahue. Instituto Andino Patagónico de Tecnologías Biológicas y Geoambientales.; Argentina. Universidad Nacional del Comahue. Centro Regional Universitario Bariloche; ArgentinaFil: Rosa, Carlos A.. Universidade Federal de Minas Gerais; BrasilFil: DeVirgilio, Jeremy. United States Department of Agriculture. Agricultural Research Service; Argentina. National Center For Agricultural; Estados UnidosFil: Hulfachor, Amanda Beth. University of Wisconsin; Estados UnidosFil: Groenewald, Marizeth. Westerdijk Fungal Biodiversity Institute; Países BajosFil: Kurtzman, Cletus P.. United States Department of Agriculture. Agricultural Research Service; Argentina. National Center For Agricultural; Estados UnidosFil: Hittinger, Chris Todd. University of Wisconsin; Estados UnidosFil: Rokas, Antonis. Vanderbilt University; Estados Unido