Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum
Open accessAbstract
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.
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The genomes of 343 yeast/fungi species combined with comprehensive genome annotations were publicly available in a previous study.
“In a previous study, the genomes of 343 yeast/fungi species combined with comprehensive genome annotations were publicly available 63 .”
From Deep learning-based kcat prediction enables improved enzyme-constrained model reconstruction (2022) · cites this paper as [63]
The Taxon sampling section identifies 343 species in total: 332 budding yeasts and 11 outgroup fungi. The Genome annotation and Data and Software Availability sections say that genome assemblies and annotations were made publicly available for the budding yeasts, but do not establish that annotations for all 11 outgroups were also made available. Thus the claim's total of 343 species with publicly available genomes and annotations is not fully supported. (LLM, conf=0.88)
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Self-citationEukaryote lateral gene transfer is Lamarckian
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Outline of Fungi and fungus-like taxa
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BackgroundA genome-scale phylogeny of the kingdom Fungi
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Self-citationThe genomic consequences of hybridization
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Incongruence in the phylogenomics era
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Self-citationToward a Fully Resolved Fungal Tree of Life
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Horizontal Gene Transfer in Eukaryotes: Not if, but How Much?
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Self-citationIntegrative approaches for species delimitation in Ascomycota
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Gene gain and loss across the metazoan tree of life
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HGT is widespread in insects and contributes to male courtship in lepidopterans
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Self-citationExtensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts
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Self-citationGenome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota
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Self-citationPhylogenomic Subsampling and the Search for Phylogenetically Reliable Loci
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Trends in yeast diversity discovery
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Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts
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Self-citationOrigin and Early Evolution of the Eukaryotic Cell
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QMaker: Fast and Accurate Method to Estimate Empirical Models of Protein Evolution
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Self-citationMitochondrial ATP generation is more proteome efficient than glycolysis
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Komagataella phaffii as Emerging Model Organism in Fundamental Research
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Self-citationEukaryotic Acquisition of a Bacterial Operon
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Self-citationFermentation innovation through complex hybridization of wild and domesticated yeasts
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Self-citationComparative genomics reveals the origin of fungal hyphae and multicellularity
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Variation and selection on codon usage bias across an entire subphylum
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Self-citationHorizontal gene transfer in eukaryotes: aligning theory with data
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Interspecific hybridization as a driver of fungal evolution and adaptation
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Cellulose- and xylan-degrading yeasts: Enzymes, applications and biotechnological potential
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Domestication reprogrammed the budding yeast life cycle
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From bumblebee to bioeconomy: Recent developments and perspectives for sophorolipid biosynthesis
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Taxonomy of Pathogenic Yeasts Candida, Cryptococcus, Malassezia, and Trichosporon
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Self-citationAn investigation of irreproducibility in maximum likelihood phylogenetic inference
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Self-citationHybridization and the origin of new yeast lineages
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Biotechnological Importance of Torulaspora delbrueckii: From the Obscurity to the Spotlight
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A computational screen for alternative genetic codes in over 250,000 genomes
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A yeast living ancestor reveals the origin of genomic introgressions
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A vast evolutionarily transient translatome contributes to phenotype and fitness
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Self-citationUnraveling the potential of non-conventional yeasts in biotechnology
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Classes and phyla of the kingdom Fungi
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Self-citationExpanding the Knowledge on the Skillful Yeast Cyberlindnera jadinii
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Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces
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What are the 100 most cited fungal genera?
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Self-citationExploring future applications of the apiculate yeast Hanseniaspora
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What makes Komagataella phaffii non-conventional?
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Macroevolutionary dynamics of gene family gain and loss along multicellular eukaryotic lineages
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Inference of phylogenetic trees directly from raw sequencing reads using Read2Tree
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Forecasting the number of species of asexually reproducing fungi (Ascomycota and Basidiomycota)
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Mechanisms of genome evolution in Candida albicans
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Spatial inter-centromeric interactions facilitated the emergence of evolutionary new centromeres
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Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection
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Into the wild: new yeast genomes from natural environments and new tools for their analysis
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Self-citationAncient balancing selection maintains incompatible versions of the galactose pathway in yeast
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- Authors
- Shen, X.-X., Opulente, D. A., Kominek, J., Zhou, X., Steenwyk, J. L., Buh, K. V., Haase, M. A. B., Wisecaver, J. H., Wang, M., Doering, D. T., Boudouris, J. T., Schneider, R. M., Langdon, Q. K., Ohkuma, M., Endoh, R., Takashima, M., Manabe, R.-I., Čadež, N., Libkind, D., Rosa, C. A., DeVirgilio, J., Hulfachor, A. B., Groenewald, M., Kurtzman, C. P., Hittinger, C. T., & Rokas, A.
- Affiliations
- Vanderbilt University (US)
- University of Wisconsin–Madison (US)
- South China Agricultural University (CN)
- RIKEN BioResource Research Center (JP)
- RIKEN Center for Integrative Medical Sciences (JP)
- University of Ljubljana (SI)
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- Universidade Federal de Minas Gerais (BR)
- Agricultural Research Service (US)
- Westerdijk Fungal Biodiversity Institute (NL)
- Corresponding author
- Hittinger, Chris Todd
- Rokas, Antonis
- ORCID
- Shen, Xing-Xing
- Opulente, Dana A.
- Kominek, Jacek
- Zhou, Xiaofan
- Steenwyk, Jacob L.
- Haase, Max A.B.
- Wisecaver, Jennifer H.
- Wang, Mingshuang
- Doering, Drew T.
- Langdon, Quinn K.
- Ohkuma, Moriya
- 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
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2018-11
- Volume
- 175
- Issue
- 6
- Pages
- 1533-1545.e20
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC6291210
- OpenAlex
- W2899763402
- Cited by
- 619
- References
- 112
- Citations by year
- 2026: 56 · 2025: 72 · 2024: 109 · 2023: 83 · 2022: 70 · 2021: 116 · 2020: 68 · 2019: 43 · 2018: 1
- FWCI
- 20.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
- PubMed Central (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- CONICET Digital (CONICET) (submittedVersion, cc-by-nc-sa)
- Funders
- National Science Foundation (DEB-1442113, DEB-1442148, IOS-1401682, DGE-1256259)
- DOE Great Lakes Bioenergy Research Center (DE-FC02-07ER64494, DE-SC0018409)
- Pew Charitable Trusts
- Vilas Trust Estate
- Guggenheim
- Vanderbilt
- National Key Project for Basic Research of China (2015CB150600)
- NHGRI (5T32HG002760)
- NIH (5T32GM007133)
- CONICET (PIP 392)
- FONCyT (PICT 2542)
- Universidad Nacional del Comahue (B199)
- Conselho Nacional de Desenvolvimento Científico e Tecnológico
- Fundação de Amparo a Pesquisa do Estado de Minas Gerais
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- Saccharomyces cerevisiae, Saccharomycotina, genome evolution, phylogeny, horizontal gene transfer, metabolic phenotypes, common ancestor, reductive evolution, gene loss
- MeSH terms
- Saccharomycetales, Phylogeny, Genome, Fungal, Evolution, Molecular, Gene Transfer, Horizontal
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