skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts

Abstract

Cell-cycle checkpoints and DNA repair processes protect organisms from possibly lethal mutational damage. Compared to other budding yeasts in the subphylum Saccharomycotina, we noticed that a lineage in the genus Hanseniaspora exhibited very high evolutionary rates, low Guanine–Cytosine (GC) content, small genome sizes, and lower gene numbers. To better understand Hanseniaspora evolution, we viewed 25 genomes, including 11 newly sequenced, representing 18/21 known species in the genus. Our phylogenomic analyses identify two Hanseniaspora lineages, a faster-evolving lineage (FEL), which began diversifying approximately 87 million years ago (mya), and a slower-evolving lineage (SEL), which began diversifying approximately 54 mya. Remarkably, both lineages lost genes associated with the cell cycle and genome integrity, but these losses were greater in the FEL. E.g., all species lost the cell-cycle regulator WHIskey 5 ( WHI5), and the FEL lost components of the spindle checkpoint pathway (e.g., Mitotic Arrest-Deficient 1 [ MAD1], Mitotic Arrest-Deficient 2 [ MAD2]) and DNA-damage–checkpoint pathway (e.g., Mitosis Entry Checkpoint 3 [ MEC3], RADiation sensitive 9 [RAD9]). Similarly, both lineages lost genes involved in DNA repair pathways, including the DNA glycosylase gene 3-MethylAdenine DNA Glycosylase 1 ( MAG1), which is part of the base-excision repair pathway, and the DNA photolyase gene PHotoreactivationmore » Repair deficient 1 ( PHR1), which is involved in pyrimidine dimer repair. Strikingly, the FEL lost 33 additional genes, including polymerases (i.e., POLymerase 4 [ POL4] and POL32) and telomere-associated genes (e.g., Repressor/activator site binding protein-Interacting Factor 1 [ RIF1], Replication Factor A 3 [ RFA3], Cell Division Cycle 13 [ CDC13], Pbp1p Binding Protein [ PBP2]). Echoing these losses, molecular evolutionary analyses reveal that, compared to the SEL, the FEL stem lineage underwent a burst of accelerated evolution, which resulted in greater mutational loads, homopolymer instabilities, and higher fractions of mutations associated with the common endogenously damaged base, 8-oxoguanine. We conclude that Hanseniaspora is an ancient lineage that has diversified and thrived, despite lacking many otherwise highly conserved cell-cycle and genome integrity genes and pathways, and may represent a novel, to our knowledge, system for studying cellular life without them.« less

Authors:
ORCiD logo [1];  [2];  [2]; ORCiD logo [1]; ORCiD logo [3]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [4];  [5];  [6];  [7];  [6]; ORCiD logo [2]; ORCiD logo [1];  [8]
  1. Vanderbilt Univ., Nashville, TN (United States)
  2. Univ. of Wisconsin–Madison, WI (United States); USDOE Great Lakes Bioenergy Research Center, Madison, WI (United States)
  3. South China Agricultural Univ., Guangzhou (China)
  4. Univ. of Ljubljana (Slovenia)
  5. Universidad Nacional del Comahue-CONICET, San Carlos de Bariloche, Río Negro (Argentina)
  6. US Dept. of Agriculture (USDA), Peoria, IL (United States)
  7. Univ. of Wisconsin–Madison, WI (United States)
  8. Sainsbury Lab. (United Kingdom)
Publication Date:
Research Org.:
USDOE Great Lakes Bioenergy Research Center, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation (NSF)
Contributing Org.:
Advanced Computing Center for Research and Education at Vanderbilt University, the Center for High-Throughput Computing at UW-Madison, and the UW Biotechnology Center DNA Sequencing Facility
OSTI Identifier:
1556080
Grant/Contract Number:  
SC0018409; FC02-07ER64494
Resource Type:
Accepted Manuscript
Journal Name:
PLoS biology (Online)
Additional Journal Information:
Journal Name: PLoS biology (Online); Journal Volume: 17; Journal Issue: 5; Journal ID: ISSN 1545-7885
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English

Citation Formats

Steenwyk, Jacob L., Opulente, Dana A., Kominek, Jacek, Shen, Xing-Xing, Zhou, Xiaofan, Labella, Abigail L., Bradley, Noah P., Eichman, Brandt F., Čadež, Neža, Libkind, Diego, DeVirgilio, Jeremy, Hulfachor, Amanda Beth, Kurtzman, Cletus P., Hittinger, Chris Todd, Rokas, Antonis, and Kamoun, Sophien. Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts. United States: N. p., 2019. Web. doi:10.1371/journal.pbio.3000255.
Steenwyk, Jacob L., Opulente, Dana A., Kominek, Jacek, Shen, Xing-Xing, Zhou, Xiaofan, Labella, Abigail L., Bradley, Noah P., Eichman, Brandt F., Čadež, Neža, Libkind, Diego, DeVirgilio, Jeremy, Hulfachor, Amanda Beth, Kurtzman, Cletus P., Hittinger, Chris Todd, Rokas, Antonis, & Kamoun, Sophien. Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts. United States. doi:10.1371/journal.pbio.3000255.
Steenwyk, Jacob L., Opulente, Dana A., Kominek, Jacek, Shen, Xing-Xing, Zhou, Xiaofan, Labella, Abigail L., Bradley, Noah P., Eichman, Brandt F., Čadež, Neža, Libkind, Diego, DeVirgilio, Jeremy, Hulfachor, Amanda Beth, Kurtzman, Cletus P., Hittinger, Chris Todd, Rokas, Antonis, and Kamoun, Sophien. Tue . "Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts". United States. doi:10.1371/journal.pbio.3000255. https://www.osti.gov/servlets/purl/1556080.
@article{osti_1556080,
title = {Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts},
author = {Steenwyk, Jacob L. and Opulente, Dana A. and Kominek, Jacek and Shen, Xing-Xing and Zhou, Xiaofan and Labella, Abigail L. and Bradley, Noah P. and Eichman, Brandt F. and Čadež, Neža and Libkind, Diego and DeVirgilio, Jeremy and Hulfachor, Amanda Beth and Kurtzman, Cletus P. and Hittinger, Chris Todd and Rokas, Antonis and Kamoun, Sophien},
abstractNote = {Cell-cycle checkpoints and DNA repair processes protect organisms from possibly lethal mutational damage. Compared to other budding yeasts in the subphylum Saccharomycotina, we noticed that a lineage in the genus Hanseniaspora exhibited very high evolutionary rates, low Guanine–Cytosine (GC) content, small genome sizes, and lower gene numbers. To better understand Hanseniaspora evolution, we viewed 25 genomes, including 11 newly sequenced, representing 18/21 known species in the genus. Our phylogenomic analyses identify two Hanseniaspora lineages, a faster-evolving lineage (FEL), which began diversifying approximately 87 million years ago (mya), and a slower-evolving lineage (SEL), which began diversifying approximately 54 mya. Remarkably, both lineages lost genes associated with the cell cycle and genome integrity, but these losses were greater in the FEL. E.g., all species lost the cell-cycle regulator WHIskey 5 (WHI5), and the FEL lost components of the spindle checkpoint pathway (e.g., Mitotic Arrest-Deficient 1 [MAD1], Mitotic Arrest-Deficient 2 [MAD2]) and DNA-damage–checkpoint pathway (e.g., Mitosis Entry Checkpoint 3 [MEC3], RADiation sensitive 9 [RAD9]). Similarly, both lineages lost genes involved in DNA repair pathways, including the DNA glycosylase gene 3-MethylAdenine DNA Glycosylase 1 (MAG1), which is part of the base-excision repair pathway, and the DNA photolyase gene PHotoreactivation Repair deficient 1 (PHR1), which is involved in pyrimidine dimer repair. Strikingly, the FEL lost 33 additional genes, including polymerases (i.e., POLymerase 4 [POL4] and POL32) and telomere-associated genes (e.g., Repressor/activator site binding protein-Interacting Factor 1 [RIF1], Replication Factor A 3 [RFA3], Cell Division Cycle 13 [CDC13], Pbp1p Binding Protein [PBP2]). Echoing these losses, molecular evolutionary analyses reveal that, compared to the SEL, the FEL stem lineage underwent a burst of accelerated evolution, which resulted in greater mutational loads, homopolymer instabilities, and higher fractions of mutations associated with the common endogenously damaged base, 8-oxoguanine. We conclude that Hanseniaspora is an ancient lineage that has diversified and thrived, despite lacking many otherwise highly conserved cell-cycle and genome integrity genes and pathways, and may represent a novel, to our knowledge, system for studying cellular life without them.},
doi = {10.1371/journal.pbio.3000255},
journal = {PLoS biology (Online)},
number = 5,
volume = 17,
place = {United States},
year = {2019},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:

Works referenced in this record:

Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants the Keio collection
journal, February 2006

  • Baba, Tomoya; Ara, Takeshi; Hasegawa, Miki
  • Molecular Systems Biology, Vol. 2, Article No. 2006.0008
  • DOI: 10.1038/msb4100050