The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae

[EN] The cell central metabolism has been shaped throughout evolutionary times when facing challenges from the availability of resources. In the budding yeast, Saccharomyces cerevisiae, a set of duplicated genes originating from an ancestral whole-genome and several coetaneous small-scale duplicatio...

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Authors: Mattenberger, Florian, Fares Riaño, Mario Ali, Toft, Christina, Sabater-Muñoz, B|||0000-0002-0301-215X
Format: article
Publication Date:2021
Country:España
Institution:Universitat Politècnica de València (UPV)
Repository:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
Language:English
OAI Identifier:oai:riunet.upv.es:10251/186213
Online Access:https://riunet.upv.es/handle/10251/186213
Access Level:Open access
Keyword:Whole-genome duplicates
Small-scale duplicates
Phenotypic response
Metabolic distance
Acidic stress
Reactive oxygen response
Heat-shock proteins
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spelling The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiaeMattenberger, FlorianFares Riaño, Mario AliToft, ChristinaSabater-Muñoz, B|||0000-0002-0301-215XWhole-genome duplicatesSmall-scale duplicatesPhenotypic responseMetabolic distanceAcidic stressReactive oxygen responseHeat-shock proteins[EN] The cell central metabolism has been shaped throughout evolutionary times when facing challenges from the availability of resources. In the budding yeast, Saccharomyces cerevisiae, 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 S. cerevisiae 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.This research was funded by Spanish National Plan for Scientific and Technical Research and Innovation from the Spanish Ministry of Economy and Competitiveness (MINECOFEDER), actually the Ministry of Science and Innovation (MCIN), Spanish Research Agency (AEI), MCIN/AEI/10.13039/501100011033 and ERDF A way of making Europe (FEDER "Una forma de hacer Europa") with grant number BFU2015-66073-P (to M.A.F.) and Generalitat Valenciana, Conselleria de Innovacion, Universidades y Sociedad Digital with grant number SEJI/2018/046 (to C.T.). F.M. was supported by a Spanish PhD Fellowship number FPI BES-2016-076677, from MCIN/AEI/10.13039/501100011033 and ESF "Investing in your future".MDPI AGGeneralitat ValencianaEuropean Regional Development FundMinisterio de Economía y CompetitividadRepositorio Institucional de la Universitat Politècnica de València Riunet20212021-11-01journal articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://riunet.upv.es/handle/10251/186213reponame:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valénciainstname:Universitat Politècnica de València (UPV)InglésengMinisterio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 BFU2015-66073-P CARACTERIZANDO LOS MECANISMOS DE INNOVACION POR DUPLICACION GENICAGeneralitat Valenciana https://doi.org/10.13039/501100003359 SEJI%2F2018%2F046Ministerio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 BES-2016-076677open accesshttp://purl.org/coar/access_right/c_abf2Reconocimiento (by)http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:riunet.upv.es:10251/1862132026-06-13T07:49:27Z
dc.title.none.fl_str_mv The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae
title The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae
spellingShingle The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae
Mattenberger, Florian
Whole-genome duplicates
Small-scale duplicates
Phenotypic response
Metabolic distance
Acidic stress
Reactive oxygen response
Heat-shock proteins
title_short The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae
title_full The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae
title_fullStr The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae
title_full_unstemmed The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae
title_sort The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae
dc.creator.none.fl_str_mv Mattenberger, Florian
Fares Riaño, Mario Ali
Toft, Christina
Sabater-Muñoz, B|||0000-0002-0301-215X
author Mattenberger, Florian
author_facet Mattenberger, Florian
Fares Riaño, Mario Ali
Toft, Christina
Sabater-Muñoz, B|||0000-0002-0301-215X
author_role author
author2 Fares Riaño, Mario Ali
Toft, Christina
Sabater-Muñoz, B|||0000-0002-0301-215X
author2_role author
author
author
dc.contributor.none.fl_str_mv Generalitat Valenciana
European Regional Development Fund
Ministerio de Economía y Competitividad
Repositorio Institucional de la Universitat Politècnica de València Riunet
dc.subject.none.fl_str_mv Whole-genome duplicates
Small-scale duplicates
Phenotypic response
Metabolic distance
Acidic stress
Reactive oxygen response
Heat-shock proteins
topic Whole-genome duplicates
Small-scale duplicates
Phenotypic response
Metabolic distance
Acidic stress
Reactive oxygen response
Heat-shock proteins
description [EN] The cell central metabolism has been shaped throughout evolutionary times when facing challenges from the availability of resources. In the budding yeast, Saccharomyces cerevisiae, 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 S. cerevisiae 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.
publishDate 2021
dc.date.none.fl_str_mv 2021
2021-11-01
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://riunet.upv.es/handle/10251/186213
url https://riunet.upv.es/handle/10251/186213
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv Ministerio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 BFU2015-66073-P CARACTERIZANDO LOS MECANISMOS DE INNOVACION POR DUPLICACION GENICA
Generalitat Valenciana https://doi.org/10.13039/501100003359 SEJI%2F2018%2F046
Ministerio de Economía y Competitividad http://dx.doi.org/10.13039/501100003329 BES-2016-076677
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Reconocimiento (by)
http://creativecommons.org/licenses/by/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Reconocimiento (by)
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv MDPI AG
publisher.none.fl_str_mv MDPI AG
dc.source.none.fl_str_mv reponame:RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
instname:Universitat Politècnica de València (UPV)
instname_str Universitat Politècnica de València (UPV)
reponame_str RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
collection RiuNet. Repositorio Institucional de la Universitat Politécnica de Valéncia
repository.name.fl_str_mv
repository.mail.fl_str_mv
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