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 PHotoreactivation Repair deficient 1 (PHR1), whichmore »
- Publication Date:
- Research Org.:
- Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); 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:
- 1630352
- Alternate Identifier(s):
- OSTI ID: 1556080
- Grant/Contract Number:
- BER DE-FC02-07ER64494 and DE-SC0018409; SC0018409; FC02-07ER64494
- Resource Type:
- Published Article
- 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 (PLoS)
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
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, ed., 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, ed., Sophien. Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts. United States. https://doi.org/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, ed., Sophien. Tue .
"Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts". United States. https://doi.org/10.1371/journal.pbio.3000255.
@article{osti_1630352,
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, ed., 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 = {Tue May 21 00:00:00 EDT 2019},
month = {Tue May 21 00:00:00 EDT 2019}
}
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