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Environmental systems biology of cold-tolerant phenotype in Saccharomyces species adapted to grow at different temperatures
Temperature is one of the leading factors that drive adaptation of organisms and ecosystems. Remarkably, many closely related species share the same habitat because of their different temporal or micro-spatial thermal adaptation. In this study, we seek to find the underlying molecular mechanisms of...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BlackWell Publishing Ltd
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4283049/ https://www.ncbi.nlm.nih.gov/pubmed/25243355 http://dx.doi.org/10.1111/mec.12930 |
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author | Paget, Caroline Mary Schwartz, Jean-Marc Delneri, Daniela |
author_facet | Paget, Caroline Mary Schwartz, Jean-Marc Delneri, Daniela |
author_sort | Paget, Caroline Mary |
collection | PubMed |
description | Temperature is one of the leading factors that drive adaptation of organisms and ecosystems. Remarkably, many closely related species share the same habitat because of their different temporal or micro-spatial thermal adaptation. In this study, we seek to find the underlying molecular mechanisms of the cold-tolerant phenotype of closely related yeast species adapted to grow at different temperatures, namely S. kudriavzevii CA111 (cryo-tolerant) and S. cerevisiae 96.2 (thermo-tolerant). Using two different systems approaches, i. thermodynamic-based analysis of a genome-scale metabolic model of S. cerevisiae and ii. large-scale competition experiment of the yeast heterozygote mutant collection, genes and pathways important for the growth at low temperature were identified. In particular, defects in lipid metabolism, oxidoreductase and vitamin pathways affected yeast fitness at cold. Combining the data from both studies, a list of candidate genes was generated and mutants for two predicted cold-favouring genes, GUT2 and ADH3, were created in two natural isolates. Compared with the parental strains, these mutants showed lower fitness at cold temperatures, with S. kudriavzevii displaying the strongest defect. Strikingly, in S. kudriavzevii, these mutations also significantly improve the growth at warm temperatures. In addition, overexpression of ADH3 in S. cerevisiae increased its fitness at cold. These results suggest that temperature-induced redox imbalances could be compensated by increased glycerol accumulation or production of cytosolic acetaldehyde through the deletion of GUT2 or ADH3, respectively. |
format | Online Article Text |
id | pubmed-4283049 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | BlackWell Publishing Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-42830492015-01-15 Environmental systems biology of cold-tolerant phenotype in Saccharomyces species adapted to grow at different temperatures Paget, Caroline Mary Schwartz, Jean-Marc Delneri, Daniela Mol Ecol Original Articles Temperature is one of the leading factors that drive adaptation of organisms and ecosystems. Remarkably, many closely related species share the same habitat because of their different temporal or micro-spatial thermal adaptation. In this study, we seek to find the underlying molecular mechanisms of the cold-tolerant phenotype of closely related yeast species adapted to grow at different temperatures, namely S. kudriavzevii CA111 (cryo-tolerant) and S. cerevisiae 96.2 (thermo-tolerant). Using two different systems approaches, i. thermodynamic-based analysis of a genome-scale metabolic model of S. cerevisiae and ii. large-scale competition experiment of the yeast heterozygote mutant collection, genes and pathways important for the growth at low temperature were identified. In particular, defects in lipid metabolism, oxidoreductase and vitamin pathways affected yeast fitness at cold. Combining the data from both studies, a list of candidate genes was generated and mutants for two predicted cold-favouring genes, GUT2 and ADH3, were created in two natural isolates. Compared with the parental strains, these mutants showed lower fitness at cold temperatures, with S. kudriavzevii displaying the strongest defect. Strikingly, in S. kudriavzevii, these mutations also significantly improve the growth at warm temperatures. In addition, overexpression of ADH3 in S. cerevisiae increased its fitness at cold. These results suggest that temperature-induced redox imbalances could be compensated by increased glycerol accumulation or production of cytosolic acetaldehyde through the deletion of GUT2 or ADH3, respectively. BlackWell Publishing Ltd 2014-11 2014-10-21 /pmc/articles/PMC4283049/ /pubmed/25243355 http://dx.doi.org/10.1111/mec.12930 Text en © 2014 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd. http://creativecommons.org/licenses/by/3.0/ This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Original Articles Paget, Caroline Mary Schwartz, Jean-Marc Delneri, Daniela Environmental systems biology of cold-tolerant phenotype in Saccharomyces species adapted to grow at different temperatures |
title | Environmental systems biology of cold-tolerant phenotype in Saccharomyces species adapted to grow at different temperatures |
title_full | Environmental systems biology of cold-tolerant phenotype in Saccharomyces species adapted to grow at different temperatures |
title_fullStr | Environmental systems biology of cold-tolerant phenotype in Saccharomyces species adapted to grow at different temperatures |
title_full_unstemmed | Environmental systems biology of cold-tolerant phenotype in Saccharomyces species adapted to grow at different temperatures |
title_short | Environmental systems biology of cold-tolerant phenotype in Saccharomyces species adapted to grow at different temperatures |
title_sort | environmental systems biology of cold-tolerant phenotype in saccharomyces species adapted to grow at different temperatures |
topic | Original Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4283049/ https://www.ncbi.nlm.nih.gov/pubmed/25243355 http://dx.doi.org/10.1111/mec.12930 |
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