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Rapid selection response to ethanol in Saccharomyces eubayanus emulates the domestication process under brewing conditions
Although the typical genomic and phenotypic changes that characterize the evolution of organisms under the human domestication syndrome represent textbook examples of rapid evolution, the molecular processes that underpin such changes are still poorly understood. Domesticated yeasts for brewing, whe...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8913853/ https://www.ncbi.nlm.nih.gov/pubmed/33755311 http://dx.doi.org/10.1111/1751-7915.13803 |
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author | Mardones, Wladimir Villarroel, Carlos A. Abarca, Valentina Urbina, Kamila Peña, Tomás A. Molinet, Jennifer Nespolo, Roberto F. Cubillos, Francisco A. |
author_facet | Mardones, Wladimir Villarroel, Carlos A. Abarca, Valentina Urbina, Kamila Peña, Tomás A. Molinet, Jennifer Nespolo, Roberto F. Cubillos, Francisco A. |
author_sort | Mardones, Wladimir |
collection | PubMed |
description | Although the typical genomic and phenotypic changes that characterize the evolution of organisms under the human domestication syndrome represent textbook examples of rapid evolution, the molecular processes that underpin such changes are still poorly understood. Domesticated yeasts for brewing, where short generation times and large phenotypic and genomic plasticity were attained in a few generations under selection, are prime examples. To experimentally emulate the lager yeast domestication process, we created a genetically complex (panmictic) artificial population of multiple Saccharomyces eubayanus genotypes, one of the parents of lager yeast. Then, we imposed a constant selection regime under a high ethanol concentration in 10 replicated populations during 260 generations (6 months) and compared them with propagated controls exposed solely to glucose. Propagated populations exhibited a selection differential of 60% in growth rate in ethanol, mostly explained by the proliferation of a single lineage (CL248.1) that competitively displaced all other clones. Interestingly, the outcome does not require the entire time‐course of adaptation, as four lineages monopolized the culture at generation 120. Sequencing demonstrated that de novo genetic variants were produced in all propagated lines, including SNPs, aneuploidies, INDELs and translocations. In addition, the different propagated populations showed correlated responses resembling the domestication syndrome: genomic rearrangements, faster fermentation rates, lower production of phenolic off‐flavours and lower volatile compound complexity. Expression profiling in beer wort revealed altered expression levels of genes related to methionine metabolism, flocculation, stress tolerance and diauxic shift, likely contributing to higher ethanol and fermentation stress tolerance in the evolved populations. Our study shows that experimental evolution can rebuild the brewing domestication process in ‘fast motion’ in wild yeast, and also provides a powerful tool for studying the genetics of the adaptation process in complex populations. |
format | Online Article Text |
id | pubmed-8913853 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-89138532022-03-17 Rapid selection response to ethanol in Saccharomyces eubayanus emulates the domestication process under brewing conditions Mardones, Wladimir Villarroel, Carlos A. Abarca, Valentina Urbina, Kamila Peña, Tomás A. Molinet, Jennifer Nespolo, Roberto F. Cubillos, Francisco A. Microb Biotechnol Research Articles Although the typical genomic and phenotypic changes that characterize the evolution of organisms under the human domestication syndrome represent textbook examples of rapid evolution, the molecular processes that underpin such changes are still poorly understood. Domesticated yeasts for brewing, where short generation times and large phenotypic and genomic plasticity were attained in a few generations under selection, are prime examples. To experimentally emulate the lager yeast domestication process, we created a genetically complex (panmictic) artificial population of multiple Saccharomyces eubayanus genotypes, one of the parents of lager yeast. Then, we imposed a constant selection regime under a high ethanol concentration in 10 replicated populations during 260 generations (6 months) and compared them with propagated controls exposed solely to glucose. Propagated populations exhibited a selection differential of 60% in growth rate in ethanol, mostly explained by the proliferation of a single lineage (CL248.1) that competitively displaced all other clones. Interestingly, the outcome does not require the entire time‐course of adaptation, as four lineages monopolized the culture at generation 120. Sequencing demonstrated that de novo genetic variants were produced in all propagated lines, including SNPs, aneuploidies, INDELs and translocations. In addition, the different propagated populations showed correlated responses resembling the domestication syndrome: genomic rearrangements, faster fermentation rates, lower production of phenolic off‐flavours and lower volatile compound complexity. Expression profiling in beer wort revealed altered expression levels of genes related to methionine metabolism, flocculation, stress tolerance and diauxic shift, likely contributing to higher ethanol and fermentation stress tolerance in the evolved populations. Our study shows that experimental evolution can rebuild the brewing domestication process in ‘fast motion’ in wild yeast, and also provides a powerful tool for studying the genetics of the adaptation process in complex populations. John Wiley and Sons Inc. 2021-03-23 /pmc/articles/PMC8913853/ /pubmed/33755311 http://dx.doi.org/10.1111/1751-7915.13803 Text en © 2021 The Authors. Microbial Biotechnology published by Society for Applied Microbiology and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made. |
spellingShingle | Research Articles Mardones, Wladimir Villarroel, Carlos A. Abarca, Valentina Urbina, Kamila Peña, Tomás A. Molinet, Jennifer Nespolo, Roberto F. Cubillos, Francisco A. Rapid selection response to ethanol in Saccharomyces eubayanus emulates the domestication process under brewing conditions |
title | Rapid selection response to ethanol in Saccharomyces eubayanus emulates the domestication process under brewing conditions |
title_full | Rapid selection response to ethanol in Saccharomyces eubayanus emulates the domestication process under brewing conditions |
title_fullStr | Rapid selection response to ethanol in Saccharomyces eubayanus emulates the domestication process under brewing conditions |
title_full_unstemmed | Rapid selection response to ethanol in Saccharomyces eubayanus emulates the domestication process under brewing conditions |
title_short | Rapid selection response to ethanol in Saccharomyces eubayanus emulates the domestication process under brewing conditions |
title_sort | rapid selection response to ethanol in saccharomyces eubayanus emulates the domestication process under brewing conditions |
topic | Research Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8913853/ https://www.ncbi.nlm.nih.gov/pubmed/33755311 http://dx.doi.org/10.1111/1751-7915.13803 |
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