The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae
Abstract
:1. Introduction
2. Results
2.1. Lactic Acid as a Non-Fermentable Carbon Source Affects S. cerevisiae Growth Parameters
2.2. Transcriptional Response of S. cerevisiae to Lactic Acid/Lactate as Non-Fermentable Carbon Source
2.3. Many Cellular Processes Are Altered When S. cerevisiae Is Challenged with Lactic Acid/Lactate
2.4. The Implication of Duplicated Genes in the Transcriptional Response of S. cerevisiae to Lactic Acid/Lactate
2.5. The Cellular Re-Programming in Response to Lactic Acid/Lactate Is Driven through Duplicated Genes
2.6. Chaperones, Heat Shock Proteins and Stress-Related Proteins Responding to Lactic Acid/Lactate as Carbon Source
2.7. Metabolic Evolution of YPL Adapted S. cerevisiae Populations
3. Discussion
3.1. Lactic Acid as Non-Fermentable Carbon Source Affects S. cerevisiae Growth Parameters
3.2. Lactic Acid as a Non-Fermentable Carbon Source Affects S. cerevisiae Transcriptomic Response
3.3. Ancient Duplicates Direct the Transcriptomic Response
3.4. Lactic Acid/Lactate as the Sole Carbon Source Induces More Than a Single Stress Response
4. Materials and Methods
4.1. Yeast Strain, Culture and Adaptive Experimental Evolution
4.2. Growth Characterization under Lactic Acid Use as Sole Carbon Source
4.3. RNAseq and Transcriptomic Profiling
4.4. Identification of Duplicated Genes Involved in the Usage of Lactic Acid as Sole Carbon Source and Their Response to Acidic Stress
4.5. Metabolic Distance between Populations
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Rodrigues, F.; Ludovico, P.; Leão, C. Sugar metabolism in yeasts: An overview of aerobic and anaerobic glucose catabolism. In Biodiversity and Ecophysiology of Yeasts; Péter, G., Rosa, C., Eds.; Springer: Berlin/Heidelberg, Germany, 2006; pp. 101–121. ISBN 978-3-540-30985-7. [Google Scholar]
- Smets, B.; Ghillebert, R.; De Snijder, P.; Binda, M.; Swinnen, E.; De Virgilio, C.; Winderickx, J. Life in the midst of scarcity: Adaptations to nutrient availability in Saccharomyces cerevisiae. Curr. Genet. 2010, 56, 1–32. [Google Scholar] [CrossRef] [Green Version]
- Pereira, R.; Wei, Y.; Mohamed, E.; Radi, M.; Malina, C.; Herrgård, M.J.; Feist, A.M.; Nielsen, J.; Chen, Y. Adaptive laboratory evolution of tolerance to dicarboxylic acids in Saccharomyces cerevisiae. Metab. Eng. 2019, 56, 130–141. [Google Scholar] [CrossRef]
- Hallsworth, J.E. Stress-free microbes lack vitality. Fungal Biol. 2018, 122, 379–385. [Google Scholar] [CrossRef] [PubMed]
- Wolfe, K.H.; Shields, D.C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 1997, 387, 708–713. [Google Scholar] [CrossRef] [PubMed]
- Marcet-Houben, M.; Gabaldón, T. Beyond the whole-genome duplication: Phylogenetic evidence for an ancient interspecies hybridization in the baker’s yeast lineage. PLoS Biol. 2015, 13, e1002220. [Google Scholar] [CrossRef] [Green Version]
- Nepi, M.; Calabrese, D.; Guarnieri, M.; Giordano, E. Evolutionary and ecological considerations on nectar-mediated tripartite interactions in angiosperms and their relevance in the mediterranean basin. Plants 2021, 10, 507. [Google Scholar] [CrossRef] [PubMed]
- Dashko, S.; Zhou, N.; Compagno, C.; Piškur, J. Why, when, and how did yeast evolve alcoholic fermentation? FEMS Yeast Res. 2014, 14, 826–832. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hagman, A.; Piškur, J. A study on the fundamental mechanism and the evolutionary driving forces behind aerobic fermentation in yeast. PLoS ONE 2015, 10, 1–24. [Google Scholar] [CrossRef]
- Wolfe, K.H. Origin of the yeast whole-genome duplication. PLoS Biol. 2015, 13, e1002221. [Google Scholar] [CrossRef] [Green Version]
- Macías, L.G.; Morard, M.; Toft, C.; Barrio, E. Comparative genomics between Saccharomyces kudriavzevii and S. cerevisiae applied to identify mechanisms involved in adaptation. Front. Genet. 2019, 10, 187. [Google Scholar] [CrossRef] [PubMed]
- Morard, M.; Benavent-Gil, Y.; Ortiz-Tovar, G.; Pérez-Través, L.; Querol, A.; Toft, C.; Barrio, E. Genome structure reveals the diversity of mating mechanisms in Saccharomyces cerevisiae x Saccharomyces kudriavzevii hybrids, and the genomic instability that promotes phenotypic diversity. Microb. Genom. 2020, 6, e000333. [Google Scholar] [CrossRef]
- Morard, M.; Ibáñez, C.; Adam, A.C.; Querol, A.; Barrio, E.; Toft, C. Genomic instability in an interspecific hybrid of the genus Saccharomyces: A matter of adaptability. Microb. Genom. 2020, 6, mgen000448. [Google Scholar] [CrossRef]
- Ohno, S. Evolution by Gene Duplication; Springer: New York, NY, USA, 1970; ISBN 978-3-642-86661-6. [Google Scholar]
- Hakes, L.; Pinney, J.W.; Lovell, S.C.; Oliver, S.G.; Robertson, D.L. All duplicates are not equal: The difference between small-scale and genome duplication. Genome Biol. 2007, 8, R209. [Google Scholar] [CrossRef]
- Farrè, D.; Albà, M.M. Heterogeneous patterns of gene-expression diversification in mammalian gene duplicates. Mol. Biol. Evol. 2010, 27, 325–335. [Google Scholar] [CrossRef] [Green Version]
- Plata, G.; Vitkup, D. Genetic robustness and functional evolution of gene duplicates. Nucleic Acids Res. 2014, 42, 2405–2414. [Google Scholar] [CrossRef] [PubMed]
- Toll-Riera, M.; San Millan, A.; Wagner, A.; MacLean, R.C. The genomic basis of evolutionary innovation in Pseudomonas aeruginosa. PLoS Genet. 2016, 12, 1–21. [Google Scholar] [CrossRef] [PubMed]
- Zhao, T.; Zwaenepoel, A.; Xue, J.Y.; Kao, S.M.; Li, Z.; Schranz, M.E.; Van de Peer, Y. Whole-genome microsynteny-based phylogeny of Angiosperms. Nat. Commun. 2021, 12, 1–14. [Google Scholar] [CrossRef]
- Fares, M.A. Survival and innovation: The role of mutational robustness in evolution. Biochimie 2015, 119, 254–261. [Google Scholar] [CrossRef] [Green Version]
- Fares, M.A.; Keane, O.M.; Toft, C.; Carretero-Paulet, L.; Jones, G.W. The roles of whole-genome and small-scale duplications in the functional specialization of Saccharomyces cerevisiae Genes. PLoS Genet. 2013, 9, e1003176. [Google Scholar] [CrossRef] [Green Version]
- Keane, O.M.; Toft, C.; Carretero-Paulet, L.; Jones, G.W.; Fares, M.A. Preservation of genetic and regulatory robustness in ancient gene duplicates of Saccharomyces cerevisiae. Genome Res. 2014, 24, 1830–1841. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fares, M.A.; Sabater-Muñoz, B.; Toft, C. Genome mutational and transcriptional hotspots are traps for duplicated genes and sources of adaptations. Genome Biol. Evol. 2017, 9, 1229–1240. [Google Scholar] [CrossRef] [Green Version]
- Mattenberger, F.; Sabater-Muñoz, B.; Toft, C.; Sablok, G.; Fares, M.A. Expression properties exhibit correlated patterns with the fate of duplicated genes, their divergence, and transcriptional plasticity in Saccharomycotina. DNA Res. 2017, 24, 559–570. [Google Scholar] [CrossRef] [Green Version]
- Khaladkar, M.; Hannenhalli, S. Functional divergence of gene duplicates—A domain-centric view. BMC Evol. Biol. 2012, 12, 126. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sabater-Muñoz, B.; Mattenberger, F.; Fares, M.A.; Toft, C. Transcriptional rewiring, adaptation, and the role of gene duplication in the metabolism of ethanol of Saccharomyces cerevisiae. mSystems 2020, 5, e00416-20. [Google Scholar] [CrossRef]
- Mattenberger, F.; Sabater-Muñoz, B.; Hallsworth, J.E.; Fares, M.A. Glycerol stress in Saccharomyces cerevisiae: Cellular responses and evolved adaptations. Environ. Microbiol. 2017, 19, 990–1007. [Google Scholar] [CrossRef] [PubMed]
- Skoneczny, M.; Skoneczna, A. Response mechanisms to chemical and physical stresses in yeast and filamentous fungi. In Stress Response Mechanisms in Fungi: Theoretical and Practical Aspects; Skoneczny, M., Ed.; Springer International Publishing: Cham, Switzerland, 2018; pp. 35–85. ISBN 978-3-030-00682-2. [Google Scholar]
- Casal, M.; Paiva, S.; Queirós, O.; Soares-Silva, I. Transport of carboxylic acids in yeasts. FEMS Microbiol. Rev. 2008, 32, 974–994. [Google Scholar] [CrossRef] [Green Version]
- Pereira, R.; Mohamed, E.T.; Radi, M.S.; Herrgård, M.J.; Feist, A.M.; Nielsen, J.; Chen, Y. Elucidating aromatic acid tolerance at low pH in Saccharomyces cerevisiae using adaptive laboratory evolution. Proc. Natl. Acad. Sci. USA 2020, 117, 27954–27961. [Google Scholar] [CrossRef]
- Jarboe, L.R.; Royce, L.A.; Liu, P. Understanding biocatalyst inhibition by carboxylic acids. Front. Microbiol. 2013, 4, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Sprouffske, K.; Wagner, A. Growthcurver: An R package for obtaining interpretable metrics from microbial growth curves. BMC Bioinform. 2016, 17, 172. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Conway, J.R.; Lex, A.; Gehlenborg, N. UpSetR: An R package for the visualization of intersecting sets and their properties. Bioinformatics 2017, 33, 2938–2940. [Google Scholar] [CrossRef] [Green Version]
- Yu, G.; Wang, L.G.; Han, Y.; He, Q.Y. ClusterProfiler: An R package for comparing biological themes among gene clusters. OMICS J. Integr. Biol. 2012, 16, 284–287. [Google Scholar] [CrossRef]
- Carretero-Paulet, L.; Albert, V.A.; Fares, M.A. Molecular evolutionary mechanisms driving functional diversification of the HSP90A family of heat shock proteins in eukaryotes. Mol. Biol. Evol. 2013, 30, 2035–2043. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Skoneczny, M. Stress Response Mechanisms in Fungi; Springer International Publishing: Cham, Switzerland, 2018; ISBN 978-3-030-00682-2. [Google Scholar]
- Brooks, G.A. The science and translation of lactate shuttle theory. Cell Metab. 2018, 27, 757–785. [Google Scholar] [CrossRef] [Green Version]
- Kiran, D.; Basaraba, R.J. Lactate metabolism and signaling in tuberculosis and cancer: A comparative review. Front. Cell. Infect. Microbiol. 2021, 11, 1–24. [Google Scholar] [CrossRef]
- Gladden, L.B. Lactate metabolism: A new paradigm for the third millennium. J. Physiol. 2004, 558, 5–30. [Google Scholar] [CrossRef]
- Dong, S.; Qian, L.; Cheng, Z.; Chen, C.; Wang, K.; Hu, S.; Zhang, X.; Wu, T. Lactate and myocadiac energy metabolism. Front. Physiol. 2021, 12, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Piper, P.; Calderon, C.O.; Hatzixanthis, K.; Mollapour, M. Weak acid adaptation: The stress response that confers yeasts with resistance to organic acid food preservatives. Microbiology 2001, 147, 2635–2642. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Venkataram, S.; Dunn, B.; Li, Y.; Agarwala, A.; Chang, J.; Ebel, E.R.; Geiler-Samerotte, K.; Hérissant, L.; Blundell, J.R.; Levy, S.F.; et al. Development of a comprehensive genotype-to-fitness map of adaptation-driving mutations in yeast. Cell 2016, 166, 1585–1596.e22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baek, S.H.; Kwon, E.Y.; Bae, S.J.; Cho, B.R.; Kim, S.Y.; Hahn, J.S. Improvement of d-Lactic acid production in Saccharomyces cerevisiae under acidic conditions by evolutionary and rational metabolic engineering. Biotechnol. J. 2017, 12, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Filteau, M.; Hamel, V.; Pouliot, M.; Gagnon-Arsenault, I.; Dubé, A.K.; Landry, C.R. Evolutionary rescue by compensatory mutations is constrained by genomic and environmental backgrounds. Mol. Syst. Biol. 2015, 11, 832. [Google Scholar] [CrossRef]
- Rosenberg, S.M. Evolving responsively: Adaptive mutation. Nat. Rev. Genet. 2001, 2, 504–515. [Google Scholar] [CrossRef] [PubMed]
- Payen, C.; Sunshine, A.B.; Ong, G.T.; Pogachar, J.L.; Zhao, W.; Dunham, M.J. High-throughput identification of adaptive mutations in experimentally evolved yeast populations. PLoS Genet. 2016, 12, e1006339. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fisher, K.J.; Buskirk, S.W.; Vignogna, R.C.; Marad, D.A.; Lang, G.I. Adaptive genome duplication affects patterns of molecular evolution in Saccharomyces cerevisiae. PLoS Genet. 2018, 14, e1007396. [Google Scholar] [CrossRef] [PubMed]
- Buskirk, S.W.; Rokes, A.B.; Lang, G.I. Adaptive evolution of nontransitive fitness in yeast. eLife 2020, 9, e62238. [Google Scholar] [CrossRef]
- Zan, Y.; Carlborg, Ö. Dissecting the genetic regulation of yeast growth plasticity in response to environmental changes. Genes 2020, 11, 1279. [Google Scholar] [CrossRef]
- Petrizzelli, M.S.; de Vienne, D.; Nidelet, T.; Noûs, C.; Dillmann, C. Data integration uncovers the metabolic bases of phenotypic variation in yeast. PLoS Comput. Biol. 2021, 17, e1009157. [Google Scholar] [CrossRef]
- Hewitt, S.K.; Foster, D.S.; Dyer, P.S.; Avery, S.V. Phenotypic heterogeneity in fungi: Importance and methodology. Fungal Biol. Rev. 2016, 30, 176–184. [Google Scholar] [CrossRef]
- Yi, X.; Dean, A.M. Phenotypic plasticity as an adaptation to a functional trade-off. eLife 2016, 5, e19307. [Google Scholar] [CrossRef]
- Pacheco, A.; Talaia, G.; Sá-Pessoa, J.; Bessa, D.; Gonçalves, M.J.; Moreira, R.; Paiva, S.; Casal, M.; Queirós, O. Lactic acid production in Saccharomyces cerevisiae is modulated by expression of the monocarboxylate transporters Jen1 and Ady2. FEMS Yeast Res. 2012, 12, 375–381. [Google Scholar] [CrossRef]
- Dato, L.; Berterame, N.M.; Ricci, M.A.; Paganoni, P.; Palmieri, L.; Porro, D.; Branduardi, P. Changes in SAM2 expression affect lactic acid tolerance and lactic acid production in Saccharomyces cerevisiae. Microb. Cell Fact. 2014, 13, 147. [Google Scholar] [CrossRef] [Green Version]
- Kang, K.; Bergdahl, B.; MacHado, D.; Dato, L.; Han, T.L.; Li, J.; Villas-Boas, S.; Herrgård, M.J.; Förster, J.; Panagiotou, G. Linking genetic, metabolic, and phenotypic diversity among Saccharomyces cerevisiae strains using multi-omics associations. Gigascience 2019, 8, giz015. [Google Scholar] [CrossRef] [Green Version]
- Ferea, T.L.; Botstein, D.; Brown, P.O.; Rosenzweig, R.F. Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc. Natl. Acad. Sci. USA 1999, 96, 9721–9726. [Google Scholar] [CrossRef] [Green Version]
- Taymaz-Nikerel, H.; Cankorur-Cetinkaya, A.; Kirdar, B. Genome-wide transcriptional response of Saccharomyces cerevisiae to stress-induced perturbations. Front. Bioeng. Biotechnol. 2016, 4, 17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Turcotte, B.; Liang, X.B.; Robert, F.; Soontorngun, N. Transcriptional regulation of nonfermentable carbon utilization in budding yeast. FEMS Yeast Res. 2010, 10, 2–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gasmi, N.; Jacques, P.E.; Klimova, N.; Guo, X.; Ricciardi, A.; Robert, F.; Turcotte, B. The switch from fermentation to respiration in Saccharomyces cerevisiae is regulated by the Ert1 transcriptional activator/repressor. Genetics 2014, 198, 547–560. [Google Scholar] [CrossRef] [PubMed]
- Ortiz-Merino, R.A.; Kuanyshev, N.; Byrne, K.P.; Varela, J.A.; Morrissey, J.P.; Porro, D.; Wolfe, K.H.; Branduardi, P. Transcriptional response to lactic acid stress in the hybrid yeast Zygosaccharomyces parabailii. Appl. Environ. Microbiol. 2017, 84, e02294-17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, J. Evolution by gene duplication: An update. Trends Ecol. Evol. 2003, 18, 292–298. [Google Scholar] [CrossRef] [Green Version]
- Cui, L.; Wall, P.K.; Leebens-Mack, J.H.; Lindsay, B.G.; Soltis, D.E.; Doyle, J.J.; Soltis, P.S.; Carlson, J.E.; Arumuganathan, K.; Barakat, A.; et al. Widespread genome duplications throughout the history of flowering plants. Genome Res. 2006, 16, 738–749. [Google Scholar] [CrossRef] [Green Version]
- Panchy, N.; Lehti-Shiu, M.; Shiu, S. Evolution of gene duplication in plants. Plant Physiol. 2016, 171, 2294–2316. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jaillon, O.; Aury, J.M.; Wincker, P. “Changing by doubling”, the impact of whole genome duplications in the evolution of eukaryotes. Comptes Rendus Biol. 2009, 332, 241–253. [Google Scholar] [CrossRef]
- Freeling, M.; Thomas, B.C. Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res. 2006, 16, 805–814. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Voordeckers, K.; Verstrepen, K.J. Experimental evolution of the model eukaryote Saccharomyces cerevisiae yields insight into the molecular mechanisms underlying adaptation. Curr. Opin. Microbiol. 2015, 28, 1–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stern, S.; Dror, T.; Stolovicki, E.; Brenner, N.; Braun, E. Genome-wide transcriptional plasticity underlies cellular adaptation to novel challenge. Mol. Syst. Biol. 2007, 3, 106. [Google Scholar] [CrossRef]
- Nguyen Ba, A.N.; Cvijović, I.; Rojas Echenique, J.I.; Lawrence, K.R.; Rego-Costa, A.; Liu, X.; Levy, S.F.; Desai, M.M. High-resolution lineage tracking reveals travelling wave of adaptation in laboratory yeast. Nature 2019, 575, 494–499. [Google Scholar] [CrossRef] [PubMed]
- Dejean, L.; Beauvoit, B.; Guérin, B.; Rigoulet, M. Growth of the yeast Saccharomyces cerevisiae on a non-fermentable substrate: Control of energetic yield by the amount of mitochondria. Biochim. Biophys. Acta Bioenerg. 2000, 1457, 45–56. [Google Scholar] [CrossRef] [Green Version]
- Orij, R.; Brul, S.; Smits, G.J. Intracellular pH is a tightly controlled signal in yeast. Biochim. Biophys. Acta Gen. Subj. 2011, 1810, 933–944. [Google Scholar] [CrossRef]
- Bergthorsson, U.; Andersson, D.I.; Roth, J.R. Ohno’s dilemma: Evolution of new genes under continuous selection. Proc. Natl. Acad. Sci. USA 2007, 104, 17004–17009. [Google Scholar] [CrossRef] [Green Version]
- Maslov, S.; Sneppen, K.; Eriksen, K.A.; Yan, K.-K. Upstream plasticity and downstream robustness in evolution of molecular networks. BMC Evol. Biol. 2004, 4, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- R Core Team. R: A Language and Environment for Statistical Computing; R Core Team: Vienna, Austria, 2020. [Google Scholar]
- Mattenberger, F.; Sabater-Muñoz, B.; Toft, C.; Fares, M.A. The phenotypic plasticity of duplicated genes in Saccharomyces cerevisiae and the origin of adaptations. G3 Genes Genomes Genet. 2017, 7, 63–75. [Google Scholar] [CrossRef] [Green Version]
- Robinson, M.D.; McCarthy, D.J.; Smyth, G.K. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26, 139–140. [Google Scholar] [CrossRef] [Green Version]
- Byrne, K.P.; Wolfe, K.H. The Yeast Gene Order Browser: Combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res. 2005, 15, 1456–1461. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Altered | Up-Regulated | Down-Regulated | |||||||
---|---|---|---|---|---|---|---|---|---|
t0–t100 | t0–t110 | t100–t110 | t0–t100 | t0–t110 | t100–t110 | t0–t100 | t0–t110 | t100–t110 | |
All | 0.1914 | 0.3713 | 0.5359 | 0.3295 | 0.2897 | 0.2890 | 0.6082 | 0.4021 | 0.9278 |
Singletons | 0.3302 | 0.5934 | 0.3585 | 0.3028 | 0.2611 | 0.1549 | 0.5000 | 0.4789 | 1.0000 |
Duplicates | 0.4955 | 0.1279 | 0.8488 | 0.2466 | 0.4028 | 0.5694 | 0.9048 | 0.1684 | 0.9365 |
WGDs | 0.3962 | 0.0132 | 0.9623 | 0.0667 | 0.5652 | 0.6522 | 0.8750 | 0.0435 | 0.9464 |
SSDs | 0.4815 | 0.7692 | 0.7037 | 0.5641 | 0.5455 | 0.3636 | 0.8667 | 0.5111 | 0.9000 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mattenberger, F.; Fares, M.A.; Toft, C.; Sabater-Muñoz, B. The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae. Int. J. Mol. Sci. 2021, 22, 12293. https://doi.org/10.3390/ijms222212293
Mattenberger F, Fares MA, Toft C, Sabater-Muñoz B. The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae. International Journal of Molecular Sciences. 2021; 22(22):12293. https://doi.org/10.3390/ijms222212293
Chicago/Turabian StyleMattenberger, Florian, Mario A. Fares, Christina Toft, and Beatriz Sabater-Muñoz. 2021. "The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae" International Journal of Molecular Sciences 22, no. 22: 12293. https://doi.org/10.3390/ijms222212293