Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss

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

doi:10.1093/genetics/iyaa012

Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss

Journal Article · Fri Nov 27 00:00:00 EST 2020 · Genetics (Online)

DOI:https://doi.org/10.1093/genetics/iyaa012· OSTI ID:1764714

Haase, Max A. B. ^[1]; Kominek, Jacek ^[2]; Opulente, Dana A. ^[2]; Shen, Xing-Xing ^[3]; LaBella, Abigail L. ^[4]; Zhou, Xiaofan ^[5]; DeVirgilio, Jeremy ^[6]; Hulfachor, Amanda Beth ^[2]; Kurtzman, Cletus P. ^[6]; Rokas, Antonis ^[4]; Hittinger, Chris Todd ^[2]

Univ. of Wisconsin, Madison, WI (United States); NYU Langone Health, NY (United States); University of Wisconsin-Madison Laboratory of Genetics
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)

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.

View Accepted Manuscript (DOE)

Research Organization:: Great Lakes Bioenergy Research Center, Madison, WI (United States)

Sponsoring Organization:: National Science Foundation; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: FC02-07ER64494; SC0018409

OSTI ID:: 1764714

Journal Information:: Genetics (Online), Journal Name: Genetics (Online) Journal Issue: 2 Vol. 217; ISSN 1943-2631

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (69)

Extensive loss of cell cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts Steenwyk, Jacob Figshare https://doi.org/10.6084/m9.figshare.7670756	collection	January 2019
MAFFT: Iterative Refinement and Additional Methods Katoh, Kazutaka; Standley, Daron M. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-646-7_8	book	January 2013
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum Shen, Xing-Xing; Opulente, Dana A.; Kominek, Jacek Cell, Vol. 175, Issue 6 https://doi.org/10.1016/j.cell.2018.10.023	journal	November 2018
Eukaryotic Acquisition of a Bacterial Operon Kominek, Jacek; Doering, Drew T.; Opulente, Dana A. Cell, Vol. 176, Issue 6 https://doi.org/10.1016/j.cell.2019.01.034	journal	March 2019
Transcriptional Rewiring of Fungal Galactose-Metabolism Circuitry Martchenko, Mikhail; Levitin, Anastasia; Hogues, Herve Current Biology, Vol. 17, Issue 12 https://doi.org/10.1016/j.cub.2007.05.017	journal	June 2007
Pseudogenization and Resurrection of a Speciation Gene Esfeld, Korinna; Berardi, Andrea E.; Moser, Michel Current Biology, Vol. 28, Issue 23 https://doi.org/10.1016/j.cub.2018.10.019	journal	December 2018
Reverse Evolution of a Classic Gene Network in Yeast Offers a Competitive Advantage Duan, Shou-Fu; Shi, Jun-Yan; Yin, Qi Current Biology, Vol. 29, Issue 7 https://doi.org/10.1016/j.cub.2019.02.038	journal	April 2019
Genomics and the making of yeast biodiversity Hittinger, Chris Todd; Rokas, Antonis; Bai, Feng-Yan Current Opinion in Genetics & Development, Vol. 35 https://doi.org/10.1016/j.gde.2015.10.008	journal	December 2015
New insights into galactose metabolism by Schizosaccharomyces pombe: Isolation and characterization of a galactose-assimilating mutant Matsuzawa, Tomohiko; Fujita, Yasuko; Tanaka, Naotaka Journal of Bioscience and Bioengineering, Vol. 111, Issue 2 https://doi.org/10.1016/j.jbiosc.2010.10.007	journal	February 2011
Acquisition of prokaryotic genes by fungal genomes Marcet-Houben, Marina; Gabaldón, Toni Trends in Genetics, Vol. 26, Issue 1 https://doi.org/10.1016/j.tig.2009.11.007	journal	January 2010
Evolutionary Transition of GAL Regulatory Circuit from Generalist to Specialist Function in Ascomycetes Choudhury, Baharul I.; Whiteway, Malcolm Trends in Microbiology, Vol. 26, Issue 8 https://doi.org/10.1016/j.tim.2017.12.008	journal	August 2018
Reversing opinions on Dollo’s Law Collin, Rachel; Miglietta, Maria Pia Trends in Ecology & Evolution, Vol. 23, Issue 11 https://doi.org/10.1016/j.tree.2008.06.013	journal	November 2008
Common lizards break Dollo’s law of irreversibility: Genome-wide phylogenomics support a single origin of viviparity and re-evolution of oviparity Recknagel, Hans; Kamenos, Nicholas A.; Elmer, Kathryn R. Molecular Phylogenetics and Evolution, Vol. 127 https://doi.org/10.1016/j.ympev.2018.05.029	journal	October 2018
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
Loss and recovery of wings in stick insects Whiting, Michael F.; Bradler, Sven; Maxwell, Taylor Nature, Vol. 421, Issue 6920 https://doi.org/10.1038/nature01313	journal	January 2003
Genome evolution in yeasts Dujon, Bernard; Sherman, David; Fischer, Gilles Nature, Vol. 430, Issue 6995 https://doi.org/10.1038/nature02579	journal	July 2004
Gene duplication and the adaptive evolution of a classic genetic switch Hittinger, Chris Todd; Carroll, Sean B. Nature, Vol. 449, Issue 7163 https://doi.org/10.1038/nature06151	journal	October 2007
Remarkably ancient balanced polymorphisms in a multi-locus gene network Hittinger, Chris Todd; Gonçalves, Paula; Sampaio, José Paulo Nature, Vol. 464, Issue 7285 https://doi.org/10.1038/nature08791	journal	February 2010
Inferring ancient divergences requires genes with strong phylogenetic signals Salichos, Leonidas; Rokas, Antonis Nature, Vol. 497, Issue 7449 https://doi.org/10.1038/nature12130	journal	May 2013
Horizontal gene transfer in eukaryotic evolution Keeling, Patrick J.; Palmer, Jeffrey D. Nature Reviews Genetics, Vol. 9, Issue 8 https://doi.org/10.1038/nrg2386	journal	August 2008
The birth, evolution and death of metabolic gene clusters in fungi Rokas, Antonis; Wisecaver, Jennifer H.; Lind, Abigail L. Nature Reviews Microbiology, Vol. 16, Issue 12 https://doi.org/10.1038/s41579-018-0075-3	journal	September 2018
Transcriptional control of the GAL/MEL regulon of yeast Saccharomyces cerevisiae: mechanism of galactose-mediated signal transduction Bhat, P. Jayadeva; Murthy, T. V. S. Molecular Microbiology, Vol. 40, Issue 5 https://doi.org/10.1046/j.1365-2958.2001.02421.x	journal	June 2001
Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts Hittinger, C. T.; Rokas, A.; Carroll, S. B. Proceedings of the National Academy of Sciences, Vol. 101, Issue 39 https://doi.org/10.1073/pnas.0404319101	journal	September 2004
Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi Slot, J. C.; Rokas, A. Proceedings of the National Academy of Sciences, Vol. 107, Issue 22 https://doi.org/10.1073/pnas.0914418107	journal	May 2010
Estimating divergence times in large molecular phylogenies Tamura, K.; Battistuzzi, F. U.; Billing-Ross, P. Proceedings of the National Academy of Sciences, Vol. 109, Issue 47 https://doi.org/10.1073/pnas.1213199109	journal	November 2012
Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides Alexander, William G.; Wisecaver, Jennifer H.; Rokas, Antonis Proceedings of the National Academy of Sciences, Vol. 113, Issue 15 https://doi.org/10.1073/pnas.1517242113	journal	March 2016
Comparative genomics of biotechnologically important yeasts Riley, Robert; Haridas, Sajeet; Wolfe, Kenneth H. Proceedings of the National Academy of Sciences, Vol. 113, Issue 35 https://doi.org/10.1073/pnas.1603941113	journal	August 2016
A Rapid Bootstrap Algorithm for the RAxML Web Servers Stamatakis, Alexandros; Hoover, Paul; Rougemont, Jacques Systematic Biology, Vol. 57, Issue 5 https://doi.org/10.1080/10635150802429642	journal	October 2008
QUAST: quality assessment tool for genome assemblies Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay Bioinformatics, Vol. 29, Issue 8 https://doi.org/10.1093/bioinformatics/btt086	journal	February 2013
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Clade- and species-specific features of genome evolution in the Saccharomycetaceae Wolfe, Kenneth H.; Armisén, David; Proux-Wera, Estelle FEMS Yeast Research, Vol. 15, Issue 5 https://doi.org/10.1093/femsyr/fov035	journal	June 2015
Novel Information Theory-Based Measures for Quantifying Incongruence among Phylogenetic Trees Salichos, Leonidas; Stamatakis, Alexandros; Rokas, Antonis Molecular Biology and Evolution, Vol. 31, Issue 5 https://doi.org/10.1093/molbev/msu061	journal	February 2014
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
Computing the Internode Certainty and Related Measures from Partial Gene Trees Kobert, Kassian; Salichos, Leonidas; Rokas, Antonis Molecular Biology and Evolution, Vol. 33, Issue 6 https://doi.org/10.1093/molbev/msw040	journal	February 2016
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro Molecular Biology and Evolution, Vol. 33, Issue 7 https://doi.org/10.1093/molbev/msw054	journal	March 2016
Fast Coalescent-Based Computation of Local Branch Support from Quartet Frequencies Sayyari, Erfan; Mirarab, Siavash Molecular Biology and Evolution, Vol. 33, Issue 7 https://doi.org/10.1093/molbev/msw079	journal	April 2016
Adaptation of S. cerevisiae to Fermented Food Environments Reveals Remarkable Genome Plasticity and the Footprints of Domestication Legras, Jean-Luc; Galeote, Virginie; Bigey, Frédéric Molecular Biology and Evolution, Vol. 35, Issue 7 https://doi.org/10.1093/molbev/msy066	journal	May 2018
DAMBE7: New and Improved Tools for Data Analysis in Molecular Biology and Evolution Xia, Xuhua Molecular Biology and Evolution, Vol. 35, Issue 6 https://doi.org/10.1093/molbev/msy073	journal	April 2018
Repeated Cis-Regulatory Tuning of a Metabolic Bottleneck Gene during Evolution Kuang, Meihua Christina; Kominek, Jacek; Alexander, William G. Molecular Biology and Evolution, Vol. 35, Issue 8 https://doi.org/10.1093/molbev/msy102	journal	May 2018
MEME SUITE: tools for motif discovery and searching Bailey, T. L.; Boden, M.; Buske, F. A. Nucleic Acids Research, Vol. 37, Issue Web Server https://doi.org/10.1093/nar/gkp335	journal	May 2009
Dollo's law and the re–evolution of shell coiling Collin, R.; Cipriani, R. Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 270, Issue 1533 https://doi.org/10.1098/rspb.2003.2517	journal	December 2003
Phylogenetic Evidence for a Major Reversal of Life-History Evolution in Plethodontid Salamanders Chippindale, Paul T.; Bonett, Ronald M.; Baldwin, Andrew S. Evolution, Vol. 58, Issue 12 https://doi.org/10.1111/j.0014-3820.2004.tb01632.x	journal	December 2004
Evidence for the Reversibility of Digit Loss: a Phylogenetic Study of limb Evolution in Bachia (Gymnophthalmidae: Squamata) Kohlsdorf, Tiana; Wagner, Günter P. Evolution, Vol. 60, Issue 9 https://doi.org/10.1111/j.0014-3820.2006.tb00533.x	journal	September 2006
Rates and Patterns in the Evolution of Snake-Like body form in Squamate Reptiles: Evidence for Repeated Re-Evolution of lost Digits and Long-Term Persistence of Intermediate body Forms Brandley, Matthew C.; Huelsenbeck, John P.; Wiens, John J. Evolution, Vol. 62, Issue 8 https://doi.org/10.1111/j.1558-5646.2008.00430.x	journal	August 2008
DID EGG-LAYING BOAS BREAK DOLLO'S LAW? PHYLOGENETIC EVIDENCE FOR REVERSAL TO OVIPARITY IN SAND BOAS ( ERYX : BOIDAE) Lynch, Vincent J.; Wagner, Günter P. Evolution, Vol. 64, Issue 1 https://doi.org/10.1111/j.1558-5646.2009.00790.x	journal	January 2010
Re-Evolution of lost Mandibular Teeth in Frogs After more than 200 Million Years, and Re-Evaluating Dollo'S law: Trait Re-Evolution in Frogs Wiens, John J. Evolution, Vol. 65, Issue 5 https://doi.org/10.1111/j.1558-5646.2011.01221.x	journal	January 2011
Horizontal gene transfer in fungi Fitzpatrick, David A. FEMS Microbiology Letters, Vol. 329, Issue 1 https://doi.org/10.1111/j.1574-6968.2011.02465.x	journal	December 2011
A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae. Johnston, M. Microbiological Reviews, Vol. 51, Issue 4 https://doi.org/10.1128/MR.51.4.458-476.1987	journal	January 1987
A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae. Johnston, M. Microbiological Reviews, Vol. 51, Issue 4 https://doi.org/10.1128/mr.51.4.458-476.1987	journal	January 1987
Motif Enrichment Analysis: a unified framework and an evaluation on ChIP data McLeay, Robert C.; Bailey, Timothy L. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-165	journal	April 2010
On the reversibility of parasitism: adaptation to a free-living lifestyle via gene acquisitions in the diplomonad Trepomonas sp. PC1 Xu, Feifei; Jerlström-Hultqvist, Jon; Kolisko, Martin BMC Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12915-016-0284-z	journal	August 2016
Factors driving metabolic diversity in the budding yeast subphylum Opulente, Dana A.; Rollinson, Emily J.; Bernick-Roehr, Cleome BMC Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12915-018-0498-3	journal	March 2018
Extensive loss of cell-cycle and DNA repair genes in an ancient lineage of bipolar budding yeasts Steenwyk, Jacob L.; Opulente, Dana A.; Kominek, Jacek PLOS Biology, Vol. 17, Issue 5 https://doi.org/10.1371/journal.pbio.3000255	journal	May 2019
The Evolution of Fungal Metabolic Pathways Wisecaver, Jennifer H.; Slot, Jason C.; Rokas, Antonis PLoS Genetics, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pgen.1004816	journal	December 2014
Variation and selection on codon usage bias across an entire subphylum LaBella, Abigail L.; Opulente, Dana A.; Steenwyk, Jacob L. PLOS Genetics, Vol. 15, Issue 7 https://doi.org/10.1371/journal.pgen.1008304	journal	July 2019
In Silico Whole Genome Sequencer and Analyzer (iWGS): a Computational Pipeline to Guide the Design and Analysis of de novo Genome Sequencing Studies Zhou, Xiaofan; Peris, David; Kominek, Jacek G3: Genes\|Genomes\|Genetics, Vol. 6, Issue 11 https://doi.org/10.1534/g3.116.034249	journal	September 2016
Reconstructing the Backbone of the Saccharomycotina Yeast Phylogeny Using Genome-Scale Data Shen, Xing-Xing; Zhou, Xiaofan; Kominek, Jacek G3: Genes\|Genomes\|Genetics, Vol. 6, Issue 12 https://doi.org/10.1534/g3.116.034744	journal	September 2016
The Reacquisition of Biotin Prototrophy in Saccharomyces cerevisiae Involved Horizontal Gene Transfer, Gene Duplication and Gene Clustering Hall, Charles; Dietrich, Fred S. Genetics, Vol. 177, Issue 4 https://doi.org/10.1534/genetics.107.074963	journal	December 2007
Genetic Basis of a Violation of Dollo’s Law: Re-Evolution of Rotating Sex Combs in Drosophila bipectinata Seher, Thaddeus D.; Ng, Chen Siang; Signor, Sarah A. Genetics, Vol. 192, Issue 4 https://doi.org/10.1534/genetics.112.145524	journal	October 2012
Fungal metabolic gene clustersâ€”caravans traveling across genomes and environments Wisecaver, Jennifer H.; Rokas, Antonis Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00161	journal	March 2015
Repeated loss of an anciently horizontally transferred gene cluster in Botrytis Campbell, Matthew A.; Staats, Martijn; van Kan, Jan A. L. Mycologia, Vol. 105, Issue 5 https://doi.org/10.3852/12-390	journal	September 2013
ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes Mirarab, Siavash; Warnow, Tandy Dryad https://doi.org/10.6076/d10c7c	dataset	January 2023
Factors driving metabolic diversity in the budding yeast subphylum [Supplemental Data] Opulente, Dana; Rollinson, Emily; Hulfachor, Amanda figshare-Supplementary information for journal article at DOI: 10.1186/s12915-018-0498-3, 16 files https://doi.org/10.6084/m9.figshare.c.4021309	collection	March 2018
Variation and selection on codon usage bias across an entire subphylum LaBella, Abigail; Opulente, Dana; Steenwyk, Jacob Figshare https://doi.org/10.6084/m9.figshare.c.4498292	collection	January 2019
The Major Features of Evolution Simpson, George Gaylord https://doi.org/10.7312/simp93764	book	December 1953
Transcriptional rewiring over evolutionary timescales changes quantitative and qualitative properties of gene expression Dalal, Chiraj K.; Zuleta, Ignacio A.; Mitchell, Kaitlin F. eLife, Vol. 5 https://doi.org/10.7554/eLife.18981	journal	September 2016
Ongoing resolution of duplicate gene functions shapes the diversification of a metabolic network Kuang, Meihua Christina; Hutchins, Paul D.; Russell, Jason D. eLife, Vol. 5 https://doi.org/10.7554/eLife.19027	journal	September 2016
Evidence for loss and reacquisition of alcoholic fermentation in a fructophilic yeast lineage Gonçalves, Carla; Wisecaver, Jennifer H.; Kominek, Jacek eLife, Vol. 7 https://doi.org/10.7554/eLife.33034	journal	April 2018

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59 BASIC BIOLOGICAL SCIENCES
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Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss

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