Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum
Abstract
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. In this study, 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.
- Authors:
-
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- Vanderbilt Univ., Nashville, TN (United States)
- Univ. of Wisconsin, Madison, WI (United States)
- Vanderbilt Univ., Nashville, TN (United States); South China Agricultural University, Guangzhou (China)
- Univ. of Wisconsin, Madison, WI (United States); NYU School of Medicine, New York, NY (United States)
- Vanderbilt Univ., Nashville, TN (United States); Purdue Univ., West Lafayette, IN (United States)
- Japan Collection of Microorganisms, RIKEN BioResource Research Center, Tsukuba (Japan)
- RIKEN Center for Integrative Medical Sciences, Yokohama (Japan)
- University of Ljubljana (Slovenia)
- Científicas y Técnicas (CONICET)-Universidad Nacional del Comahue (Argentina)
- Universidade Federal de Minas Gerais, Belo Horizonte, MG (Brazil)
- U.S. Department of Agriculture, Peoria, IL (United States)
- Westerdijk Fungal Biodiversity Institute, Utrecht (the Netherlands)
- Publication Date:
- Research Org.:
- Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- Contributing Org.:
- Advanced Computing Center for Research and Education at Vanderbilt University; the Center for High-Throughput Computing at the University of Wisconsin—Madison; Lucigen, the CIPRES Science Gateway; and the University of Wisconsin Biotechnology Center DNA Sequencing Facility
- OSTI Identifier:
- 1506653
- Grant/Contract Number:
- SC0018409; FC02-07ER64494
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Cell
- Additional Journal Information:
- Journal Volume: 175; Journal Issue: 6; Journal ID: ISSN 0092-8674
- Publisher:
- Elsevier
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Ascomycota; Saccharomycotina; high-throughput sequencing; genomics; phylogenetics; phylogenomics; molecular dating; horizontal gene transfer; metabolic traits; and reductive evolution
Citation Formats
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, and Rokas, Antonis. Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum. United States: N. p., 2018.
Web. doi:10.1016/j.cell.2018.10.023.
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. Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum. United States. https://doi.org/10.1016/j.cell.2018.10.023
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, and Rokas, Antonis. Thu .
"Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum". United States. https://doi.org/10.1016/j.cell.2018.10.023. https://www.osti.gov/servlets/purl/1506653.
@article{osti_1506653,
title = {Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum},
author = {Shen, Xing-Xing and Opulente, Dana A. and Kominek, Jacek and Zhou, Xiaofan and Steenwyk, Jacob L. and Buh, Kelly V. and Haase, Max A. B. and Wisecaver, Jennifer H. and Wang, Mingshuang and Doering, Drew T. and Boudouris, James T. and Schneider, Rachel M. and Langdon, Quinn K. and Ohkuma, Moriya and Endoh, Rikiya and Takashima, Masako and Manabe, Ri-ichiroh and Čadež, Neža and Libkind, Diego and Rosa, Carlos A. and DeVirgilio, Jeremy and Hulfachor, Amanda Beth and Groenewald, Marizeth and Kurtzman, Cletus P. and Hittinger, Chris Todd and Rokas, Antonis},
abstractNote = {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. In this study, 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.},
doi = {10.1016/j.cell.2018.10.023},
journal = {Cell},
number = 6,
volume = 175,
place = {United States},
year = {Thu Nov 08 00:00:00 EST 2018},
month = {Thu Nov 08 00:00:00 EST 2018}
}
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New genome assemblies reveal patterns of domestication and adaptation across Brettanomyces (Dekkera) species
journal, March 2020
- Roach, Michael J.; Borneman, Anthony R.
- BMC Genomics, Vol. 21, Issue 1
Multilayered horizontal operon transfers from bacteria reconstruct a thiamine salvage pathway in yeasts
journal, October 2019
- Gonçalves, Carla; Gonçalves, Paula
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 44
André Goffeau's imprinting on second generation yeast “genomologists”
journal, January 2019
- Fairhead, Cécile; Fischer, Gilles; Liti, Gianni
- Yeast, Vol. 36, Issue 4
Fermentation innovation through complex hybridization of wild and domesticated yeasts
journal, October 2019
- Langdon, Quinn K.; Peris, David; Baker, EmilyClare P.
- Nature Ecology & Evolution, Vol. 3, Issue 11
Variation and selection on codon usage bias across an entire subphylum
journal, July 2019
- LaBella, Abigail L.; Opulente, Dana A.; Steenwyk, Jacob L.
- PLOS Genetics, Vol. 15, Issue 7
Quantitative global studies reveal differential translational control by start codon context across the fungal kingdom
journal, February 2020
- Wallace, Edward W. J.; Maufrais, Corinne; Sales-Lee, Jade
- Nucleic Acids Research, Vol. 48, Issue 5
The renaissance of yeasts as microbial factories in the modern age of biomanufacturing
journal, September 2019
- Payen, Celia; Thompson, Dawn
- Yeast, Vol. 36, Issue 12
A Small Horizontally Transferred Gene Cluster Contributes to the Sporulation of Alternaria alternata
journal, November 2019
- Wang, Mingshuang; Fu, Huilan; Ruan, Ruoxin
- Genome Biology and Evolution, Vol. 11, Issue 12
Mycoses in northeastern Brazil: epidemiology and prevalence of fungal species in 8 years of retrospective analysis in Alagoas
journal, May 2019
- de Albuquerque Maranhão, Fernanda Cristina; Oliveira-Júnior, Jorge Belém; dos Santos Araújo, Maria Anilda
- Brazilian Journal of Microbiology, Vol. 50, Issue 4
Comparative genomics reveals the origin of fungal hyphae and multicellularity
journal, September 2019
- Kiss, Enikő; Hegedüs, Botond; Virágh, Máté
- Nature Communications, Vol. 10, Issue 1
Characterization of Aspergillus nidulans TRAPPs uncovers unprecedented similarities between fungi and metazoans and reveals the modular assembly of TRAPPII
journal, December 2019
- Pinar, Mario; Arias-Palomo, Ernesto; de los Ríos, Vivian
- PLOS Genetics, Vol. 15, Issue 12
A subcellular proteome atlas of the yeast Komagataella phaffii
journal, January 2020
- Valli, Minoska; Grillitsch, Karlheinz; Grünwald-Gruber, Clemens
- FEMS Yeast Research, Vol. 20, Issue 1
Quartet-Based Computations of Internode Certainty Provide Robust Measures of Phylogenetic Incongruence
journal, August 2019
- Zhou, Xiaofan; Lutteropp, Sarah; Czech, Lucas
- Systematic Biology, Vol. 69, Issue 2
Carbon source requirements for mating and mating‐type switching in the methylotrophic yeasts Ogataea (Hansenula) polymorpha and Komagataella phaffii (Pichia pastoris)
journal, December 2019
- Feng, Dahao; Stoyanov, Anton; Olliff, Juliana C.
- Yeast, Vol. 37, Issue 2
Evolution unscathed: Darwin Devolves argues on weak reasoning that unguided evolution is a destructive force, incapable of innovation
journal, February 2019
- Lang, Gregory I.; Rice, Amber M.
- Evolution, Vol. 73, Issue 4
Assembly and Analysis of the Genome Sequence of the Yeast Brettanomyces naardenensis CBS 7540
journal, October 2019
- Tiukova, Ievgeniia A.; Jiang, Huifeng; Dainat, Jacques
- Microorganisms, Vol. 7, Issue 11
Selecting for Altered Substrate Specificity Reveals the Evolutionary Flexibility of ATP-Binding Cassette Transporters
journal, May 2020
- Srikant, Sriram; Gaudet, Rachelle; Murray, Andrew W.
- Current Biology, Vol. 30, Issue 9
Stress-induced expression is enriched for evolutionarily young genes in diverse budding yeasts
journal, May 2020
- Doughty, Tyler W.; Domenzain, Iván; Millan-Oropeza, Aaron
- Nature Communications, Vol. 11, Issue 1
Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts
journal, May 2019
- Steenwyk, Jacob L.; Opulente, Dana A.; Kominek, Jacek
- PLOS Biology, Vol. 17, Issue 5
The yeast mating-type switching endonuclease HO is a domesticated member of an unorthodox homing genetic element family
journal, April 2020
- Coughlan, Aisling Y.; Lombardi, Lisa; Braun-Galleani, Stephanie
- eLife, Vol. 9
Protein evolution is structure dependent and non-homogeneous across the tree of life
conference, September 2020
- Pandey, Akanksha; Braun, Edward L.
- BCB '20: 11th ACM International Conference on Bioinformatics, Computational Biology and Health Informatics, Proceedings of the 11th ACM International Conference on Bioinformatics, Computational Biology and Health Informatics
Osh6 requires Ist2 for localization to the ER-PM contacts and efficient phosphatidylserine transport
journal, January 2020
- D'Ambrosio, Juan Martín; Albanèse, Véronique; Lipp, Nicolas-Frédéric
- Journal of Cell Science
Paralogs in the PKA Regulon Traveled Different Evolutionary Routes to Divergent Expression in Budding Yeast
journal, April 2021
- Heineike, Benjamin M.; El-Samad, Hana
- Frontiers in Fungal Biology, Vol. 2
Multiple Reinventions of Mating-type Switching during Budding Yeast Evolution
journal, August 2019
- Krassowski, Tadeusz; Kominek, Jacek; Shen, Xing-Xing
- Current Biology, Vol. 29, Issue 15
Comparative genomics reveals the origin of fungal hyphae and multicellularity
journal, September 2019
- Kiss, Enikő; Hegedüs, Botond; Virágh, Máté
- Nature Communications, Vol. 10, Issue 1
Quantitative global studies reveal differential translational control by start codon context across the fungal kingdom
journal, February 2020
- Wallace, Edward W. J.; Maufrais, Corinne; Sales-Lee, Jade
- Nucleic Acids Research, Vol. 48, Issue 5
Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts
journal, May 2019
- Steenwyk, Jacob L.; Opulente, Dana A.; Kominek, Jacek
- PLOS Biology, Vol. 17, Issue 5
Characterization of Aspergillus nidulans TRAPPs uncovers unprecedented similarities between fungi and metazoans and reveals the modular assembly of TRAPPII
journal, December 2019
- Pinar, Mario; Arias-Palomo, Ernesto; de los Ríos, Vivian
- PLOS Genetics, Vol. 15, Issue 12
Evolution of Ty1 copy number control in yeast by horizontal transfer and recombination
journal, February 2020
- Czaja, Wioletta; Bensasson, Douda; Ahn, Hyo Won
- PLOS Genetics, Vol. 16, Issue 2
An Overview of Genes From Cyberlindnera americana, a Symbiont Yeast Isolated From the Gut of the Bark Beetle Dendroctonus rhizophagus (Curculionidae: Scolytinae), Involved in the Detoxification Process Using Genome and Transcriptome Data
journal, September 2019
- Soto-Robles, L. Viridiana; Torres-Banda, Verónica; Rivera-Orduña, Flor N.
- Frontiers in Microbiology, Vol. 10
Investigation of Genetic Relationships Between Hanseniaspora Species Found in Grape Musts Revealed Interspecific Hybrids With Dynamic Genome Structures
journal, January 2020
- Saubin, Méline; Devillers, Hugo; Proust, Lucas
- Frontiers in Microbiology, Vol. 10
Assembly and Analysis of the Genome Sequence of the Yeast Brettanomyces naardenensis CBS 7540
journal, October 2019
- Tiukova, Ievgeniia A.; Jiang, Huifeng; Dainat, Jacques
- Microorganisms, Vol. 7, Issue 11