The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast <em>Saccharomyces cerevisiae</em>
The cell central metabolism has been shaped throughout evolutionary times when facing challenges from the availability of resources. In the budding yeast, <i>Saccharomyces cerevisiae</i>, a set of duplicated genes originating from an ancestral whole-genome and several coetaneous small-sc...
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MDPI AG
2021-11-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/22/22/12293 |
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| author | Florian Mattenberger Mario A. Fares Christina Toft Beatriz Sabater-Muñoz |
| author_facet | Florian Mattenberger Mario A. Fares Christina Toft Beatriz Sabater-Muñoz |
| author_sort | Florian Mattenberger |
| collection | DOAJ |
| description | The cell central metabolism has been shaped throughout evolutionary times when facing challenges from the availability of resources. In the budding yeast, <i>Saccharomyces cerevisiae</i>, a set of duplicated genes originating from an ancestral whole-genome and several coetaneous small-scale duplication events drive energy transfer through glucose metabolism as the main carbon source either by fermentation or respiration. These duplicates (~a third of the genome) have been dated back to approximately 100 MY, allowing for enough evolutionary time to diverge in both sequence and function. Gene duplication has been proposed as a molecular mechanism of biological innovation, maintaining balance between mutational robustness and evolvability of the system. However, some questions concerning the molecular mechanisms behind duplicated genes transcriptional plasticity and functional divergence remain unresolved. In this work we challenged <i>S. cerevisiae</i> to the use of lactic acid/lactate as the sole carbon source and performed a small adaptive laboratory evolution to this non-fermentative carbon source, determining phenotypic and transcriptomic changes. We observed growth adaptation to acidic stress, by reduction of growth rate and increase in biomass production, while the transcriptomic response was mainly driven by repression of the whole-genome duplicates, those implied in glycolysis and overexpression of ROS response. The contribution of several duplicated pairs to this carbon source switch and acidic stress is also discussed. |
| first_indexed | 2024-03-10T05:26:11Z |
| format | Article |
| id | doaj.art-fed7fe5371514672a83fac69999f03bc |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T05:26:11Z |
| publishDate | 2021-11-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-fed7fe5371514672a83fac69999f03bc2023-11-22T23:40:06ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-11-0122221229310.3390/ijms222212293The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast <em>Saccharomyces cerevisiae</em>Florian Mattenberger0Mario A. Fares1Christina Toft2Beatriz Sabater-Muñoz3Integrative and Systems Biology Group, Department of Abiotic Stress, Institute for Cellular and Molecular Biology of Plants (IBMCP) from the Spanish National Research Council (CSIC), Polytechnic University of Valencia (UPV), 46022 Valencia, SpainIntegrative and Systems Biology Group, Department of Abiotic Stress, Institute for Cellular and Molecular Biology of Plants (IBMCP) from the Spanish National Research Council (CSIC), Polytechnic University of Valencia (UPV), 46022 Valencia, SpainPanomics and Evolutionary Systems Microbiology Group, Program Systems Biology of Molecular Interactions and Regulation, Institute for Integrative Systems Biology (I2SysBio), Joint Institute of the Spanish National Research Council (CSIC), Universidad de Valencia (UV), 46980 Paterna, SpainIntegrative and Systems Biology Group, Department of Abiotic Stress, Institute for Cellular and Molecular Biology of Plants (IBMCP) from the Spanish National Research Council (CSIC), Polytechnic University of Valencia (UPV), 46022 Valencia, SpainThe cell central metabolism has been shaped throughout evolutionary times when facing challenges from the availability of resources. In the budding yeast, <i>Saccharomyces cerevisiae</i>, a set of duplicated genes originating from an ancestral whole-genome and several coetaneous small-scale duplication events drive energy transfer through glucose metabolism as the main carbon source either by fermentation or respiration. These duplicates (~a third of the genome) have been dated back to approximately 100 MY, allowing for enough evolutionary time to diverge in both sequence and function. Gene duplication has been proposed as a molecular mechanism of biological innovation, maintaining balance between mutational robustness and evolvability of the system. However, some questions concerning the molecular mechanisms behind duplicated genes transcriptional plasticity and functional divergence remain unresolved. In this work we challenged <i>S. cerevisiae</i> to the use of lactic acid/lactate as the sole carbon source and performed a small adaptive laboratory evolution to this non-fermentative carbon source, determining phenotypic and transcriptomic changes. We observed growth adaptation to acidic stress, by reduction of growth rate and increase in biomass production, while the transcriptomic response was mainly driven by repression of the whole-genome duplicates, those implied in glycolysis and overexpression of ROS response. The contribution of several duplicated pairs to this carbon source switch and acidic stress is also discussed.https://www.mdpi.com/1422-0067/22/22/12293whole-genome duplicatessmall-scale duplicatesphenotypic responsemetabolic distanceacidic stressreactive oxygen response |
| spellingShingle | Florian Mattenberger Mario A. Fares Christina Toft Beatriz Sabater-Muñoz The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast <em>Saccharomyces cerevisiae</em> International Journal of Molecular Sciences whole-genome duplicates small-scale duplicates phenotypic response metabolic distance acidic stress reactive oxygen response |
| title | The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast <em>Saccharomyces cerevisiae</em> |
| title_full | The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast <em>Saccharomyces cerevisiae</em> |
| title_fullStr | The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast <em>Saccharomyces cerevisiae</em> |
| title_full_unstemmed | The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast <em>Saccharomyces cerevisiae</em> |
| title_short | The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast <em>Saccharomyces cerevisiae</em> |
| title_sort | role of ancestral duplicated genes in adaptation to growth on lactate a non fermentable carbon source for the yeast em saccharomyces cerevisiae em |
| topic | whole-genome duplicates small-scale duplicates phenotypic response metabolic distance acidic stress reactive oxygen response |
| url | https://www.mdpi.com/1422-0067/22/22/12293 |
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