TY - JOUR
T1 - Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces
AU - Peris, David
AU - Ubbelohde, Emily J.
AU - Kuang, Meihua Christina
AU - Kominek, Jacek
AU - Langdon, Quinn K.
AU - Adams, Marie
AU - Koshalek, Justin A.
AU - Hulfachor, Amanda Beth
AU - Opulente, Dana A.
AU - Hall, David J.
AU - Hyma, Katie
AU - Fay, Justin C.
AU - Leducq, Jean Baptiste
AU - Charron, Guillaume
AU - Landry, Christian R.
AU - Libkind, Diego
AU - Gonçalves, Carla
AU - Gonçalves, Paula
AU - Sampaio, José Paulo
AU - Wang, Qi Ming
AU - Bai, Feng Yan
AU - Wrobel, Russel L.
AU - Hittinger, Chris Todd
N1 - info:eu-repo/grantAgreement/EC/H2020/747775/EU#
info:eu-repo/grantAgreement/EC/FP7/274337/EU#
Funding Information:
We thank the University of Wisconsin Biotechnology Center DNA Sequencing Facility for providing Illumina and Sanger sequencing facilities and services; Maria Sardi, Audrey Gasch, and Ursula Bond for providing strains; Sean McIlwain for providing guidance for genome ultrascaffolding; Yury V. Bukhman for discussing applications of the Growth Curve Analysis Tool (GCAT); Mick McGee for HPLC analysis; Raúl Ortíz-Merino for assistance during YGAP annotations; Jessica Leigh for assistance with PopART; Cecile Ané for suggestions about BUCKy utilization and phylogenetic network analyses; Samina Naseeb and Daniela Delneri for sharing preliminary multi-locus Saccharomyces jurei data; and Branden Timm, Brian Kyle, and Dan Metzger for computational assistance. Some computations were performed on Tirant III of the Spanish Supercomputing Network (“Servei d’Informàtica de la Universitat de València”) under the project BCV-2021-1-0001 granted to DP, while others were performed at the Wisconsin Energy Institute and the Center for High-Throughput Computing of the University of Wisconsin–Madison. During a portion of this project, DP was a researcher funded by the Research Council of Norway (RCN) grant Nos. RCN 324253, and the Generalitat Valenciana plan GenT grant No. CIDEGENT/2021/039. D.P. is a recipient of an Illumina Grant for Illumina Sequencing Saccharomyces strains in this study. Q.K.L. was supported by the National Science Foundation under Grant No. DGE-1256259 (Graduate Research Fellowship) and the Predoctoral Training Program in Genetics, funded by the National Institutes of Health (5T32GM007133). This material is based upon work supported in part by the Great Lakes Bioenergy Research Center, Office of Science, Office of Biological and Environmental Research under Award Numbers DE-SC0018409 and DE-FC02-07ER64494; the National Science Foundation under Grant Nos. DEB-1253634, DEB−1442148, and DEB-2110403; and the USDA National Institute of Food and Agriculture Hatch Project Number 1020204. C.T.H. is an H. I. Romnes Faculty Fellow, supported by the Office of the Vice Chancellor for Research and Graduate Education with funding from the Wisconsin Alumni Research Foundation. QMW was supported by the National Natural Science Foundation of China (NSFC) under Grant Nos. 31770018 and 31961133020. C.R.L. holds the Canada Research Chair in Cellular Systems and Synthetic Biology, and his research on wild yeast is supported by an NSERC Discovery Grant.
Publisher Copyright:
© 2023, The Author(s).
PY - 2023/12
Y1 - 2023/12
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85147724046&partnerID=8YFLogxK
U2 - 10.1038/s41467-023-36139-2
DO - 10.1038/s41467-023-36139-2
M3 - Article
C2 - 36755033
AN - SCOPUS:85147724046
SN - 2041-1723
VL - 14
JO - Nature Communications
JF - Nature Communications
IS - 1
M1 - 690
ER -