Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum

Xing-Xing Shen; Dana A Opulente; Jacek Kominek; Xiaofan Zhou; Jacob L Steenwyk; Kelly V Buh; Max A B Haase; Jennifer H Wisecaver; Mingshuang Wang; Drew T Doering; James T Boudouris; Rachel M Schneider; Quinn K Langdon; Moriya Ohkuma; Rikiya Endoh; Masako Takashima; Ri-Ichiroh Manabe; Neža Čadež; Diego Libkind; Carlos A Rosa; Jeremy DeVirgilio; Amanda Beth Hulfachor; Marizeth Groenewald; Cletus P Kurtzman; Chris Todd Hittinger; Antonis Rokas

doi:10.1016/j.cell.2018.10.023

Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum

Cell. 2018 Nov 29;175(6):1533-1545.e20. doi: 10.1016/j.cell.2018.10.023. Epub 2018 Nov 8.

Authors

Xing-Xing Shen¹, Dana A Opulente², Jacek Kominek², Xiaofan Zhou³, Jacob L Steenwyk¹, Kelly V Buh⁴, Max A B Haase⁵, Jennifer H Wisecaver⁶, Mingshuang Wang¹, Drew T Doering⁴, James T Boudouris⁴, Rachel M Schneider², Quinn K Langdon⁴, Moriya Ohkuma⁷, Rikiya Endoh⁷, Masako Takashima⁷, Ri-Ichiroh Manabe⁸, Neža Čadež⁹, Diego Libkind¹⁰, Carlos A Rosa¹¹, Jeremy DeVirgilio¹², Amanda Beth Hulfachor⁴, Marizeth Groenewald¹³, Cletus P Kurtzman¹², Chris Todd Hittinger¹⁴, Antonis Rokas¹⁵

Affiliations

¹ Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA.
² 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.
³ 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.
⁴ 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.
⁵ 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.
⁶ Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA; Department of Biochemistry, Center for Plant Biology, Purdue University, West Lafayette, IN 47907, USA.
⁷ Japan Collection of Microorganisms, RIKEN BioResource Research Center, Tsukuba, Ibaraki 305-0074, Japan.
⁸ 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.
⁹ Biotechnical Faculty, University of Ljubljana, 1000 Ljubljana, Slovenia.
¹⁰ 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.
¹¹ Departamento de Microbiologia, ICB, CP 486, Universidade Federal de Minas Gerais, Belo Horizonte, MG, 31270-901, Brazil.
¹² 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.
¹³ Westerdijk Fungal Biodiversity Institute, 3584 CT, Utrecht, the Netherlands.
¹⁴ 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: cthittinger@wisc.edu.
¹⁵ Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235, USA. Electronic address: antonis.rokas@vanderbilt.edu.

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.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Evolution, Molecular*
Gene Transfer, Horizontal*
Genome, Fungal*
Phylogeny*
Saccharomycetales / classification*
Saccharomycetales / genetics*

Associated data

figshare/10.6084/m9.figshare.5854692

Abstract

Publication types

MeSH terms

Associated data

Grants and funding