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

Journal Article · · Nature Communications
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  1. Univ. of Oslo (Norway); Inst. of Agrochemistry and Food Technology (IATA), Valencia (Spain); Univ. of Wisconsin, Madison, WI (United States); University of Wisconsin-Madison Laboratory of Genetics
  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

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.

Research Organization:
Great Lakes Bioenergy Research Center, Madison, WI (United States)
Sponsoring Organization:
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)
Grant/Contract Number:
SC0018409; FC02-07ER64494
OSTI ID:
1970475
Journal Information:
Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 14; ISSN 2041-1723
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (151)

Data from: A unique ecological niche fosters hybridization of oak-tree and vineyard isolates of Saccharomyces cerevisiae. dataset January 2015
Summer temperature can predict the distribution of wild yeast populations journal January 2016
Saccharomyces yeast hybrids on the rise journal December 2021
Highly diverged lineages of Saccharomyces paradoxus in temperate to subtropical climate zones in China journal January 2022
Yeasts from temperate forests journal January 2022
ggplot2 book January 2009
SeqinR 1.0-2: A Contributed Package to the R Project for Statistical Computing Devoted to Biological Sequences Retrieval and Analysis book January 2007
Fungal mitochondrial genomes and genetic polymorphisms journal September 2018
Modeling Microbial Growth Curves with GCAT journal February 2015
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method journal October 2011
The evolving species concepts used for yeasts: from phenotypes and genomes to speciation networks journal June 2021
Basic local alignment search tool journal October 1990
Domestication and Divergence of Saccharomyces cerevisiae Beer Yeasts journal September 2016
Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum journal November 2018
Eukaryotic Acquisition of a Bacterial Operon journal March 2019
Allopatric Divergence, Secondary Contact, and Genetic Isolation in Wild Yeast Populations journal March 2007
Evidence for a Far East Asian origin of lager beer yeast journal May 2014
Reverse Evolution of a Classic Gene Network in Yeast Offers a Competitive Advantage journal April 2019
Human-associated migration of Holarctic Saccharomyces uvarum strains to Patagonia journal December 2020
‘Everything is everywhere: but the environment selects’: ubiquitous distribution and ecological determinism in microbial biogeography journal September 2008
The Power of Natural Variation for Model Organism Biology journal March 2016
The evolution of the GALactose utilization pathway in budding yeasts journal January 2022
Relaxed selection in the wild journal September 2009
The era of reference genomes in conservation genomics journal March 2022
FASconCAT: Convenient handling of data matrices journal September 2010
Mitochondrial introgression suggests extensive ancestral hybridization events among Saccharomyces species journal March 2017
Chromosomal evolution in Saccharomyces journal May 2000
Engineering evolution to study speciation in yeasts journal March 2003
Genome-scale approaches to resolving incongruence in molecular phylogenies journal October 2003
Population genomics of domestic and wild yeasts journal February 2009
Remarkably ancient balanced polymorphisms in a multi-locus gene network journal February 2010
Predictors of elevational biodiversity gradients change from single taxa to the multi-taxa community level journal December 2016
A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum journal June 2014
Comprehensive survey of condition-specific reproductive isolation reveals genetic incompatibility in yeast journal May 2015
The genomic and phenotypic diversity of Schizosaccharomyces pombe journal February 2015
Contrasting evolutionary genome dynamics between domesticated and wild yeasts journal April 2017
Speciation driven by hybridization and chromosomal plasticity in a wild yeast journal January 2016
The origin and adaptive evolution of domesticated populations of yeast from Far East Asia journal July 2018
An investigation of irreproducibility in maximum likelihood phylogenetic inference journal November 2020
Interspecific hybridization facilitates niche adaptation in beer yeast journal October 2019
Fermentation innovation through complex hybridization of wild and domesticated yeasts journal October 2019
Genome evolution across 1,011 Saccharomyces cerevisiae isolates journal April 2018
Genetic dissection of interspecific differences in yeast thermotolerance journal October 2018
Dynamics of mtDNA introgression during species range expansion: insights from an experimental longitudinal study journal July 2016
TCS: a computer program to estimate gene genealogies journal October 2000
Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts journal September 2004
Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118 journal September 2009
Population genomics and local adaptation in wild isolates of a model microbial eukaryote journal January 2011
Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast journal August 2011
Earth BioGenome Project: Sequencing life for the future of life journal April 2018
A mutant of Saccharomyces cerevisiae defective for nuclear fusion. journal October 1976
The design of Jemboss: a graphical user interface to EMBOSS journal September 2003
CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure journal May 2007
DnaSP v5: a software for comprehensive analysis of DNA polymorphism data journal April 2009
Fast and accurate short read alignment with Burrows-Wheeler transform journal May 2009
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses journal June 2009
The Sequence Alignment/Map format and SAMtools journal June 2009
BEDTools: a flexible suite of utilities for comparing genomic features journal January 2010
BUCKy: Gene tree/species tree reconciliation with Bayesian concordance analysis journal September 2010
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data journal April 2012
QUAST: quality assessment tool for genome assemblies journal February 2013
NextClip: an analysis and read preparation tool for Nextera Long Mate Pair libraries journal December 2013
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
Trimmomatic: a flexible trimmer for Illumina sequence data journal April 2014
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs journal June 2015
Qualimap 2: advanced multi-sample quality control for high-throughput sequencing data journal October 2015
ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R journal July 2018
The evolutionary history of Saccharomyces species inferred from completed mitochondrial genomes and revision in the ‘yeast mitochondrial genetic code’ journal June 2017
2μ plasmid in Saccharomyces species and in Saccharomyces cerevisiae journal October 2015
Truncation of Gal4p explains the inactivation of theGAL/MELregulon in bothSaccharomyces bayanusand someSaccharomyces cerevisiaewine strains journal September 2016
Genomic Evidence of an Ancient East Asian Divergence Event in Wild Saccharomyces cerevisiae journal January 2021
Inference of Population Structure Using Multilocus Genotype Data journal June 2000
Inference of Population Structure Using Multilocus Genotype Data: Linked Loci and Correlated Allele Frequencies journal August 2003
Repeated horizontal gene transfer of GAL actose metabolism genes violates Dollo’s law of irreversible loss journal November 2020
ASTRAL-Pro: Quartet-Based Species-Tree Inference despite Paralogy journal September 2020
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
PopGenome: An Efficient Swiss Army Knife for Population Genomic Analyses in R journal April 2014
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies journal November 2014
Evolutionary Advantage Conferred by an Eukaryote-to-Eukaryote Gene Transfer Event in Wine Yeasts journal March 2015
Extensive Horizontal Transfer and Homologous Recombination Generate Highly Chimeric Mitochondrial Genomes in Yeast journal May 2015
The Genome Sequence of Saccharomyces eubayanus and the Domestication of Lager-Brewing Yeasts journal August 2015
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets journal March 2016
Mitochondrial Recombination and Introgression during Speciation by Hybridization journal April 2017
BUSCO Applications from Quality Assessments to Gene Prediction and Phylogenomics journal December 2017
Adaptation of S. cerevisiae to Fermented Food Environments Reveals Remarkable Genome Plasticity and the Footprints of Domestication journal May 2018
Repeated Cis-Regulatory Tuning of a Metabolic Bottleneck Gene during Evolution journal May 2018
Treeio: An R Package for Phylogenetic Tree Input and Output with Richly Annotated and Associated Data journal October 2019
Nucleotide sequence and characteristics of a Ty element from yeast journal January 1985
PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments journal July 2006
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees journal April 2016
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space journal February 2012
Three new species in the Saccharomyces sensu stricto complex: Saccharomyces cariocanus, Saccharomyces kudriavzevii and Saccharomyces mikatae. journal September 2000
Saccharomyces jurei sp. nov., isolation and genetic identification of a novel yeast species from Quercus robur journal June 2017
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data journal July 2010
Phylogenetic super-networks from partial trees journal October 2004
Saccharomyces eubayanus and Saccharomyces arboricola reside in North Island native New Zealand forests journal December 2015
Phylogeography of the wild Lager-brewing ancestor ( Saccharomyces eubayanus ) in Patagonia journal October 2018
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data journal September 2016
Mechanical barriers to introgressive hybridization revealed by mitochondrial introgression patterns in Ohomopterus ground beetle assemblages journal November 2007
Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity journal August 2012
Horizontal gene transfer in fungi journal December 2011
Inferring weak population structure with the assistance of sample group information journal September 2009
S pider : An R package for the analysis of species identity and evolution, with particular reference to DNA barcoding journal January 2012
phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package journal December 2011
Population structure and reticulate evolution of Saccharomyces eubayanus and its lager-brewing hybrids journal April 2014
Chromosomal variation segregates within incipient species and correlates with reproductive isolation journal August 2014
A population genomics insight into the Mediterranean origins of wine yeast domestication journal September 2015
A unique ecological niche fosters hybridization of oak-tree and vineyard isolates of Saccharomyces cerevisiae journal November 2015
A genomic perspective on hybridization and speciation journal March 2016
Both temperature fluctuations and East Asian monsoons have driven plant diversification in the karst ecosystems from southern China journal October 2017
The role of mitochondrial introgression in illuminating the evolutionary history of Nearctic treefrogs
  • Bryson, Robert W.; Smith, Brian Tilston; Nieto-Montes de Oca, Adrian
  • Zoological Journal of the Linnean Society, Vol. 172, Issue 1 https://doi.org/10.1111/zoj.12169
journal August 2014
Mitochondria-encoded genes contribute to evolution of heat and cold tolerance in yeast journal January 2019
Mitochondrial DNA and temperature tolerance in lager yeasts journal January 2019
GENETICS: Yeast as a Model Organism journal August 1997
Ancient balancing selection maintains incompatible versions of the galactose pathway in yeast journal January 2021
Temperature Adaptation Markedly Determines Evolution within the Genus Saccharomyces journal February 2011
A pipeline for automated annotation of yeast genome sequences by a conserved-synteny approach journal January 2012
High quality de novo sequencing and assembly of the Saccharomyces arboricolus genome journal January 2013
STRUCTURE PLOT: a program for drawing elegant STRUCTURE bar plots in user friendly interface journal August 2014
An assembly and alignment-free method of phylogeny reconstruction from next-generation sequencing data journal July 2015
Discordant evolution of mitochondrial and nuclear yeast genomes at population level journal May 2020
Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production journal March 2017
taxize: taxonomic search and retrieval in R journal January 2013
Bushes in the Tree of Life journal November 2006
Multiple Molecular Mechanisms Cause Reproductive Isolation between Three Yeast Species journal July 2010
The Dynamics of Incomplete Lineage Sorting across the Ancient Adaptive Radiation of Neoavian Birds journal August 2015
A polyploid admixed origin of beer yeasts derived from European and Asian wine populations journal March 2019
Trait Variation in Yeast Is Defined by Population History journal June 2011
Inference of Population Structure using Dense Haplotype Data journal January 2012
The Probability of a Gene Tree Topology within a Phylogenetic Network with Applications to Hybridization Detection journal April 2012
Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus journal July 2016
Postglacial migration shaped the genomic diversity and global distribution of the wild ancestor of lager-brewing hybrids journal April 2020
An Out-of-Patagonia migration explains the worldwide diversity and distribution of Saccharomyces eubayanus lineages journal May 2020
Large-scale fungal strain sequencing unravels the molecular diversity in mating loci maintained by long-term balancing selection journal March 2022
Evidence for Divergent Evolution of Growth Temperature Preference in Sympatric Saccharomyces Species journal June 2011
Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement journal November 2014
The Awesome Power of Yeast Evolutionary Genetics: New Genome Sequences and Strain Resources for the Saccharomyces sensu stricto Genus journal June 2011
A Dynamic Mobile DNA Family in the Yeast Mitochondrial Genome journal June 2015
In Silico Whole Genome Sequencer and Analyzer (iWGS): a Computational Pipeline to Guide the Design and Analysis of de novo Genome Sequencing Studies journal September 2016
Reconstructing the Backbone of the Saccharomycotina Yeast Phylogeny Using Genome-Scale Data journal September 2016
Whole Genome Sequencing, de Novo Assembly and Phenotypic Profiling for the New Budding Yeast Species Saccharomyces jurei journal August 2018
Sequence Diversity, Reproductive Isolation and Species Concepts in Saccharomyces journal September 2006
Genomic Insights into the Saccharomyces sensu stricto Complex journal February 2015
Patterns of Genomic Instability in Interspecific Yeast Hybrids With Diverse Ancestries journal October 2021
Evolution of small prokaryotic genomes journal January 2015
Adaptive Gene Content and Allele Distribution Variations in the Wild and Domesticated Populations of Saccharomyces cerevisiae journal February 2021
Revisiting the Taxonomic Synonyms and Populations of Saccharomyces cerevisiae—Phylogeny, Phenotypes, Ecology and Domestication journal June 2020
HybPiper: Extracting Coding Sequence and Introns for Phylogenetics from High-Throughput Sequencing Reads Using Target Enrichment journal July 2016
Large-scale fungal strain sequencing unravels the molecular diversity in mating loci maintained by long-term balancing selection dataset January 2021
The fascinating and secret wild life of the budding yeast S. cerevisiae journal March 2015
Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network journal September 2016

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