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Title: Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces

Abstract

Species is the fundamental unit to quantify biodiversity. In recent years, the model yeast Saccharomyces cerevisiae has seen an increased number of studies related to its geographical distribution, population structure, and phenotypic diversity. However, seven additional species from the same genus have been less thoroughly studied, which has limited our understanding of the macroevolutionary events leading to the diversification of this genus over the last 20 million years. Here, we show the geographies, hosts, substrates, and phylogenetic relationships for approximately 1,800 Saccharomyces strains, covering the complete genus with unprecedented breadth and depth. We generated and analyzed complete genome sequences of 163 strains and phenotyped 128 phylogenetically diverse strains. This dataset provides insights about genetic and phenotypic diversity within and between species and populations, quantifies reticulation and incomplete lineage sorting, and demonstrates how gene flow and selection have affected traits, such as galactose metabolism. These findings elevate the genus Saccharomyces as a model to understand biodiversity and evolution in microbial eukaryotes.

Authors:
ORCiD logo [1];  [2];  [2]; ORCiD logo [2];  [2]; ORCiD logo [2];  [2];  [2];  [2];  [3];  [4];  [4];  [5]; ORCiD logo [6]; ORCiD logo [7];  [8];  [9]; ORCiD logo [10]; ORCiD logo [10]; ORCiD logo [11] more »; ORCiD logo [12]; ORCiD logo [2]; ORCiD logo [2] « less
  1. Univ. of Oslo (Norway); Inst. of Agrochemistry and Food Technology (IATA), Valencia (Spain); Univ. of Wisconsin, Madison, WI (United States)
  2. Univ. of Wisconsin, Madison, WI (United States)
  3. Univ. of Utrecht (The Netherlands)
  4. Univ. of Rochester, NY (United States)
  5. Univ. de Montréal (Canada); Univ. Laval, Quebec City (Canada)
  6. Canada Natural Resources, Quebec City (Canada)
  7. Univ. Laval, Quebec City (Canada)
  8. Científicas y Técnicas (CONICET)-Univ. Nacional del Comahue, Bariloche (Argentina)
  9. Univ. of Wisconsin, Madison, WI (United States); Univ. NOVA de Lisboa, Caparica (Portugal); Vanderbilt Univ., Nashville, TN (United States)
  10. Univ. NOVA de Lisboa, Caparica (Portugal)
  11. Univ. of Wisconsin, Madison, WI (United States); Hebei Univ., Baoding (China)
  12. Chinese Academy of Sciences (CAS), Beijing (China). Inst. of Chemistry
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); Marie Sklodowska-Curie; Research Council of Norway (RCN); Generalitat Valenciana plan GenT; National Science Foundation (NSF); National Natural Science Foundation of China (NSFC)
OSTI Identifier:
1970475
Grant/Contract Number:  
SC0018409; FC02-07ER64494; 747775; RCN 324253; 274337; CIDEGENT/2021/039; DGE-1256259; DEB-1253634; DEB−1442148; DEB-2110403; 31770018; 31961133020
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 14; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Evolutionary genetics; Food microbiology; Phylogenetics; Population genetics; Saccharomyces cerevisiae

Citation Formats

Peris, David, Ubbelohde, Emily J., Kuang, Meihua Christina, Kominek, Jacek, Langdon, Quinn K., Adams, Marie, Koshalek, Justin A., Hulfachor, Amanda Beth, Opulente, Dana A., Hall, David J., Hyma, Katie, Fay, Justin C., Leducq, Jean-Baptiste, Charron, Guillaume, Landry, Christian R., Libkind, Diego, Gonçalves, Carla, Gonçalves, Paula, Sampaio, José Paulo, Wang, Qi-Ming, Bai, Feng-Yan, Wrobel, Russel L., and Hittinger, Chris Todd. Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces. United States: N. p., 2023. Web. doi:10.1038/s41467-023-36139-2.
Peris, David, Ubbelohde, Emily J., Kuang, Meihua Christina, Kominek, Jacek, Langdon, Quinn K., Adams, Marie, Koshalek, Justin A., Hulfachor, Amanda Beth, Opulente, Dana A., Hall, David J., Hyma, Katie, Fay, Justin C., Leducq, Jean-Baptiste, Charron, Guillaume, Landry, Christian R., Libkind, Diego, Gonçalves, Carla, Gonçalves, Paula, Sampaio, José Paulo, Wang, Qi-Ming, Bai, Feng-Yan, Wrobel, Russel L., & Hittinger, Chris Todd. Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces. United States. https://doi.org/10.1038/s41467-023-36139-2
Peris, David, Ubbelohde, Emily J., Kuang, Meihua Christina, Kominek, Jacek, Langdon, Quinn K., Adams, Marie, Koshalek, Justin A., Hulfachor, Amanda Beth, Opulente, Dana A., Hall, David J., Hyma, Katie, Fay, Justin C., Leducq, Jean-Baptiste, Charron, Guillaume, Landry, Christian R., Libkind, Diego, Gonçalves, Carla, Gonçalves, Paula, Sampaio, José Paulo, Wang, Qi-Ming, Bai, Feng-Yan, Wrobel, Russel L., and Hittinger, Chris Todd. Wed . "Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces". United States. https://doi.org/10.1038/s41467-023-36139-2. https://www.osti.gov/servlets/purl/1970475.
@article{osti_1970475,
title = {Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces},
author = {Peris, David and Ubbelohde, Emily J. and Kuang, Meihua Christina and Kominek, Jacek and Langdon, Quinn K. and Adams, Marie and Koshalek, Justin A. and Hulfachor, Amanda Beth and Opulente, Dana A. and Hall, David J. and Hyma, Katie and Fay, Justin C. and Leducq, Jean-Baptiste and Charron, Guillaume and Landry, Christian R. and Libkind, Diego and Gonçalves, Carla and Gonçalves, Paula and Sampaio, José Paulo and Wang, Qi-Ming and Bai, Feng-Yan and Wrobel, Russel L. and Hittinger, Chris Todd},
abstractNote = {Species is the fundamental unit to quantify biodiversity. In recent years, the model yeast Saccharomyces cerevisiae has seen an increased number of studies related to its geographical distribution, population structure, and phenotypic diversity. However, seven additional species from the same genus have been less thoroughly studied, which has limited our understanding of the macroevolutionary events leading to the diversification of this genus over the last 20 million years. Here, we show the geographies, hosts, substrates, and phylogenetic relationships for approximately 1,800 Saccharomyces strains, covering the complete genus with unprecedented breadth and depth. We generated and analyzed complete genome sequences of 163 strains and phenotyped 128 phylogenetically diverse strains. This dataset provides insights about genetic and phenotypic diversity within and between species and populations, quantifies reticulation and incomplete lineage sorting, and demonstrates how gene flow and selection have affected traits, such as galactose metabolism. These findings elevate the genus Saccharomyces as a model to understand biodiversity and evolution in microbial eukaryotes.},
doi = {10.1038/s41467-023-36139-2},
journal = {Nature Communications},
number = 1,
volume = 14,
place = {United States},
year = {Wed Feb 08 00:00:00 EST 2023},
month = {Wed Feb 08 00:00:00 EST 2023}
}

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Reverse Evolution of a Classic Gene Network in Yeast Offers a Competitive Advantage
journal, April 2019


trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009


Extensive Horizontal Transfer and Homologous Recombination Generate Highly Chimeric Mitochondrial Genomes in Yeast
journal, May 2015

  • Wu, Baojun; Buljic, Adnan; Hao, Weilong
  • Molecular Biology and Evolution, Vol. 32, Issue 10
  • DOI: 10.1093/molbev/msv127

The design of Jemboss: a graphical user interface to EMBOSS
journal, September 2003


Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids
journal, April 2020


Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast
journal, August 2011

  • Libkind, D.; Hittinger, C. T.; Valerio, E.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 35
  • DOI: 10.1073/pnas.1105430108

Genomic Evidence of an Ancient East Asian Divergence Event in Wild Saccharomyces cerevisiae
journal, January 2021

  • Bendixsen, Devin P.; Gettle, Noah; Gilchrist, Ciaran
  • Genome Biology and Evolution, Vol. 13, Issue 2
  • DOI: 10.1093/gbe/evab001

DnaSP v5: a software for comprehensive analysis of DNA polymorphism data
journal, April 2009


BEDTools: a flexible suite of utilities for comparing genomic features
journal, January 2010


Phylogenetic super-networks from partial trees
journal, October 2004

  • Huson, D. H.; Dezulian, T.; Klopper, T.
  • IEEE/ACM Transactions on Computational Biology and Bioinformatics, Vol. 1, Issue 4
  • DOI: 10.1109/TCBB.2004.44

MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

  • Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
  • Molecular Biology and Evolution, Vol. 33, Issue 7
  • DOI: 10.1093/molbev/msw054

ASTRAL-Pro: Quartet-Based Species-Tree Inference despite Paralogy
journal, September 2020

  • Zhang, Chao; Scornavacca, Celine; Molloy, Erin K.
  • Molecular Biology and Evolution, Vol. 37, Issue 11
  • DOI: 10.1093/molbev/msaa139

The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010


FASconCAT: Convenient handling of data matrices
journal, September 2010


‘Everything is everywhere: but the environment selects’: ubiquitous distribution and ecological determinism in microbial biogeography
journal, September 2008

  • O’Malley, Maureen A.
  • Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences, Vol. 39, Issue 3
  • DOI: 10.1016/j.shpsc.2008.06.005

Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity
journal, August 2012


Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production
journal, March 2017

  • Peris, David; Moriarty, Ryan V.; Alexander, William G.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0763-7

The genomic and phenotypic diversity of Schizosaccharomyces pombe
journal, February 2015

  • Jeffares, Daniel C.; Rallis, Charalampos; Rieux, Adrien
  • Nature Genetics, Vol. 47, Issue 3
  • DOI: 10.1038/ng.3215

Domestication and Divergence of Saccharomyces cerevisiae Beer Yeasts
journal, September 2016


Inferring weak population structure with the assistance of sample group information
journal, September 2009


Speciation driven by hybridization and chromosomal plasticity in a wild yeast
journal, January 2016

  • Leducq, Jean-Baptiste; Nielly-Thibault, Lou; Charron, Guillaume
  • Nature Microbiology, Vol. 1, Issue 1
  • DOI: 10.1038/nmicrobiol.2015.3

Predictors of elevational biodiversity gradients change from single taxa to the multi-taxa community level
journal, December 2016

  • Peters, Marcell K.; Hemp, Andreas; Appelhans, Tim
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13736

Summer temperature can predict the distribution of wild yeast populations
journal, January 2016

  • Robinson, Heather A.; Pinharanda, Ana; Bensasson, Douda
  • Ecology and Evolution, Vol. 6, Issue 4
  • DOI: 10.1002/ece3.1919

Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement
journal, November 2014


A unique ecological niche fosters hybridization of oak-tree and vineyard isolates of Saccharomyces cerevisiae
journal, November 2015

  • Clowers, Katie J.; Will, Jessica L.; Gasch, Audrey P.
  • Molecular Ecology, Vol. 24, Issue 23
  • DOI: 10.1111/mec.13439

BUSCO Applications from Quality Assessments to Gene Prediction and Phylogenomics
journal, December 2017

  • Waterhouse, Robert M.; Seppey, Mathieu; Simão, Felipe A.
  • Molecular Biology and Evolution, Vol. 35, Issue 3
  • DOI: 10.1093/molbev/msx319

The Sequence Alignment/Map format and SAMtools
journal, June 2009


Chromosomal variation segregates within incipient species and correlates with reproductive isolation
journal, August 2014

  • Charron, Guillaume; Leducq, Jean-Baptiste; Landry, Christian R.
  • Molecular Ecology, Vol. 23, Issue 17
  • DOI: 10.1111/mec.12864

A genomic perspective on hybridization and speciation
journal, March 2016

  • Payseur, Bret A.; Rieseberg, Loren H.
  • Molecular Ecology, Vol. 25, Issue 11
  • DOI: 10.1111/mec.13557

Interspecific hybridization facilitates niche adaptation in beer yeast
journal, October 2019

  • Gallone, Brigida; Steensels, Jan; Mertens, Stijn
  • Nature Ecology & Evolution, Vol. 3, Issue 11
  • DOI: 10.1038/s41559-019-0997-9

An assembly and alignment-free method of phylogeny reconstruction from next-generation sequencing data
journal, July 2015


Allopatric Divergence, Secondary Contact, and Genetic Isolation in Wild Yeast Populations
journal, March 2007


Both temperature fluctuations and East Asian monsoons have driven plant diversification in the karst ecosystems from southern China
journal, October 2017

  • Kong, Hanghui; Condamine, Fabien L.; Harris, Aj
  • Molecular Ecology, Vol. 26, Issue 22
  • DOI: 10.1111/mec.14367

Nucleotide sequence and characteristics of a Ty element from yeast
journal, January 1985

  • Hauber, Joachim; Nelböck-Hochstetter, Peter; Feldmann, Horst
  • Nucleic Acids Research, Vol. 13, Issue 8
  • DOI: 10.1093/nar/13.8.2745

Inference of Population Structure using Dense Haplotype Data
journal, January 2012