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PMID: 30415838 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum.

Cell ·Vol. 175 ·No. 6 ·2018-00-29 ·Pages 1533-1545.e20

Shen XX, Opulente DA, Kominek J, Zhou X, Steenwyk JL, Buh KV, Haase MAB, Wisecaver JH, Wang M, Doering DT, Boudouris JT, Schneider RM, Langdon QK, Ohkuma M, Endoh R, Takashima M, Manabe RI, Čadež N, Libkind D, Rosa CA, DeVirgilio J, Hulfachor AB, Groenewald M, Kurtzman CP, Hittinger CT, Rokas A

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. 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.

Keywords
Ascomycota Saccharomycotina and reductive evolution genomics high-throughput sequencing horizontal gene transfer metabolic traits molecular dating phylogenetics phylogenomics
MeSH Terms
Evolution, Molecular Gene Transfer, Horizontal Genome, Fungal Phylogeny Saccharomycetales/classification,genetics
Authors & Affiliations
26 authors, click to expand affiliations / ORCID
Shen Xing-Xing
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.
Opulente Dana A
Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA.
Kominek Jacek
Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA.
Zhou Xiaofan
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA; Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, 510642 Guangzhou, China.
Steenwyk Jacob L
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.
Buh Kelly V
Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA.
Haase Max A B
Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA; Sackler Institute of Graduate Biomedical Sciences, NYU School of Medicine, New York, NY 10016, USA.
Wisecaver Jennifer H
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA; Department of Biochemistry, Center for Plant Biology, Purdue University, West Lafayette, IN 47907, USA.
Wang Mingshuang
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.
Doering Drew T
Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA.
Boudouris James T
Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA.
Schneider Rachel M
Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA.
Langdon Quinn K
Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA.
Ohkuma Moriya
Japan Collection of Microorganisms, RIKEN BioResource Research Center, Tsukuba, Ibaraki 305-0074, Japan.
Endoh Rikiya
Japan Collection of Microorganisms, RIKEN BioResource Research Center, Tsukuba, Ibaraki 305-0074, Japan.
Takashima Masako
Japan Collection of Microorganisms, RIKEN BioResource Research Center, Tsukuba, Ibaraki 305-0074, Japan.
Manabe Ri-Ichiroh
Division of Genomic Technologies, RIKEN Center For Life Science Technologies, Laboratory for Comprehensive Genomic Analysis, RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa 230-0045, Japan.
Čadež Neža
Biotechnical Faculty, University of Ljubljana, 1000 Ljubljana, Slovenia.
Libkind Diego
Laboratorio de Microbiología Aplicada y Biotecnología, Instituto Andino Patagónico de Tecnologías Biológicas y Geoambientales (IPATEC), Consejo Nacional de Investigaciones, Científicas y Técnicas (CONICET)-Universidad Nacional del Comahue, 8400 Bariloche, Argentina.
Rosa Carlos A
Departamento de Microbiologia, ICB, CP 486, Universidade Federal de Minas Gerais, Belo Horizonte, MG, 31270-901, Brazil.
DeVirgilio Jeremy
Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, U.S. Department of Agriculture, Peoria, IL 61604, USA.
Hulfachor Amanda Beth
Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA.
Groenewald Marizeth
Westerdijk Fungal Biodiversity Institute, 3584 CT, Utrecht, the Netherlands.
Kurtzman Cletus P
Mycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, U.S. Department of Agriculture, Peoria, IL 61604, USA.
Hittinger Chris Todd
Laboratory of Genetics, Genome Center of Wisconsin, Wisconsin Energy Institute, J.F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, WI 53706, USA; DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 53706, USA. Electronic address: [email protected].
Rokas Antonis
Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA. Electronic address: [email protected].
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Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
DOI
10.1016/j.cell.2018.10.023
Email
[email protected]
[email protected]
Published
2018-00-29
Epub
2018-00-08
Pages
1533-1545.e20
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC6291210
Subset
IM
Grants
NIGMS NIH HHS · T32 GM007133 · United States
NHGRI NIH HHS · T32 HG002760 · United States
Databases
figshare
10.6084/m9.figshare.5854692
External Links
PubMed source DOI: 10.1016/j.cell.2018.10.023 PMC Full Text View journal details
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