Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss
Abstract
Dollo’s law posits that evolutionary losses are irreversible, thereby narrowing the potential paths of evolutionary change. While phenotypic reversals to ancestral states have been observed, little is known about their underlying genetic causes. The genomes of budding yeasts have been shaped by extensive reductive evolution, such as reduced genome sizes and the losses of metabolic capabilities. However, the extent and mechanisms of trait reacquisition after gene loss in yeasts have not been thoroughly studied. Here, through phylogenomic analyses, we reconstructed the evolutionary history of the yeast galactose utilization pathway and observed widespread and repeated losses of the ability to utilize galactose, which occurred concurrently with the losses of GALactose (GAL) utilization genes. Unexpectedly, we detected multiple galactose-utilizing lineages that were deeply embedded within clades that underwent ancient losses of galactose utilization. We show that at least two, and possibly three, lineages reacquired the GAL pathway via yeast-to-yeast horizontal gene transfer. Our results show how trait reacquisition can occur tens of millions of years after an initial loss via horizontal gene transfer from distant relatives. Furthermore, these findings demonstrate that the losses of complex traits and even whole pathways are not always evolutionary dead-ends, highlighting how reversals to ancestral states canmore »
- Authors:
-
- Univ. of Wisconsin, Madison, WI (United States); NYU Langone Health, NY (United States)
- Univ. of Wisconsin, Madison, WI (United States)
- Vanderbilt Univ., Nashville, TN (United States); Zhejiang Univ., Hangzhou (China)
- Vanderbilt Univ., Nashville, TN (United States)
- Vanderbilt Univ., Nashville, TN (United States); South China Agricultural Univ., Guangzhou (China)
- U.S. Dept. of Agriculture, Peoria, IL (United States)
- 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)
- OSTI Identifier:
- 1764714
- Grant/Contract Number:
- SC0018409; FC02-07ER64494; DEB-1442113; DEB-1442148
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Genetics (Online)
- Additional Journal Information:
- Journal Name: Genetics (Online); Journal Volume: 217; Journal Issue: 2; Journal ID: ISSN 1943-2631
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Gene loss; evolution; GAL cluster; Dollo’s law; horizontal gene transfer; yeasts; lateral gene transfer
Citation Formats
Haase, Max A. B., Kominek, Jacek, Opulente, Dana A., Shen, Xing-Xing, LaBella, Abigail L., Zhou, Xiaofan, DeVirgilio, Jeremy, Hulfachor, Amanda Beth, Kurtzman, Cletus P., Rokas, Antonis, and Hittinger, Chris Todd. Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss. United States: N. p., 2020.
Web. doi:10.1093/genetics/iyaa012.
Haase, Max A. B., Kominek, Jacek, Opulente, Dana A., Shen, Xing-Xing, LaBella, Abigail L., Zhou, Xiaofan, DeVirgilio, Jeremy, Hulfachor, Amanda Beth, Kurtzman, Cletus P., Rokas, Antonis, & Hittinger, Chris Todd. Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss. United States. https://doi.org/10.1093/genetics/iyaa012
Haase, Max A. B., Kominek, Jacek, Opulente, Dana A., Shen, Xing-Xing, LaBella, Abigail L., Zhou, Xiaofan, DeVirgilio, Jeremy, Hulfachor, Amanda Beth, Kurtzman, Cletus P., Rokas, Antonis, and Hittinger, Chris Todd. Fri .
"Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss". United States. https://doi.org/10.1093/genetics/iyaa012. https://www.osti.gov/servlets/purl/1764714.
@article{osti_1764714,
title = {Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss},
author = {Haase, Max A. B. and Kominek, Jacek and Opulente, Dana A. and Shen, Xing-Xing and LaBella, Abigail L. and Zhou, Xiaofan and DeVirgilio, Jeremy and Hulfachor, Amanda Beth and Kurtzman, Cletus P. and Rokas, Antonis and Hittinger, Chris Todd},
abstractNote = {Dollo’s law posits that evolutionary losses are irreversible, thereby narrowing the potential paths of evolutionary change. While phenotypic reversals to ancestral states have been observed, little is known about their underlying genetic causes. The genomes of budding yeasts have been shaped by extensive reductive evolution, such as reduced genome sizes and the losses of metabolic capabilities. However, the extent and mechanisms of trait reacquisition after gene loss in yeasts have not been thoroughly studied. Here, through phylogenomic analyses, we reconstructed the evolutionary history of the yeast galactose utilization pathway and observed widespread and repeated losses of the ability to utilize galactose, which occurred concurrently with the losses of GALactose (GAL) utilization genes. Unexpectedly, we detected multiple galactose-utilizing lineages that were deeply embedded within clades that underwent ancient losses of galactose utilization. We show that at least two, and possibly three, lineages reacquired the GAL pathway via yeast-to-yeast horizontal gene transfer. Our results show how trait reacquisition can occur tens of millions of years after an initial loss via horizontal gene transfer from distant relatives. Furthermore, these findings demonstrate that the losses of complex traits and even whole pathways are not always evolutionary dead-ends, highlighting how reversals to ancestral states can occur.},
doi = {10.1093/genetics/iyaa012},
journal = {Genetics (Online)},
number = 2,
volume = 217,
place = {United States},
year = {Fri Nov 27 00:00:00 EST 2020},
month = {Fri Nov 27 00:00:00 EST 2020}
}
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