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Strong ethanol- and frequency-dependent ecological interactions in a community of wine-fermenting yeasts

Natural wine fermentation depends on a complex consortium of native microorganisms rather than inoculation of industrial yeast strains. While this diversity of yeasts can result in an increased repertoire of wine flavors and aromas, it can also result in the inhibition of Saccharomyces cerevisiae, w...

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Autores principales: Lax, Simon, Gore, Jeff
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10499898/
https://www.ncbi.nlm.nih.gov/pubmed/37704781
http://dx.doi.org/10.1038/s42003-023-05284-1
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author Lax, Simon
Gore, Jeff
author_facet Lax, Simon
Gore, Jeff
author_sort Lax, Simon
collection PubMed
description Natural wine fermentation depends on a complex consortium of native microorganisms rather than inoculation of industrial yeast strains. While this diversity of yeasts can result in an increased repertoire of wine flavors and aromas, it can also result in the inhibition of Saccharomyces cerevisiae, which is uniquely able to complete fermentation. Understanding how yeast species interact with each other within the wine-fermenting community and disentangling ecological interactions from environmental impacts on growth rates, is key to developing synthetic communities that can provide the sensory benefits of natural fermentation while lowering the risk of stuck ferments. Here, we co-culture all pairwise combinations of five commonly isolated wine-fermenting yeasts and show that competitive outcomes are a strong function of ethanol concentration, with frequency-dependent bistable interactions common at low alcohol and an increasingly transitive competitive hierarchy developing as alcohol increases. We also show that pairwise outcomes are predictive of five-species community outcomes, and that frequency dependence in pairwise interactions propagates to alternative states in the full community, highlighting the importance of species abundance as well as composition. We also observe that monoculture growth rates are only weakly predictive of competitive success, highlighting the need to incorporate ecological interactions when designing synthetic fermenting communities.
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spelling pubmed-104998982023-09-15 Strong ethanol- and frequency-dependent ecological interactions in a community of wine-fermenting yeasts Lax, Simon Gore, Jeff Commun Biol Article Natural wine fermentation depends on a complex consortium of native microorganisms rather than inoculation of industrial yeast strains. While this diversity of yeasts can result in an increased repertoire of wine flavors and aromas, it can also result in the inhibition of Saccharomyces cerevisiae, which is uniquely able to complete fermentation. Understanding how yeast species interact with each other within the wine-fermenting community and disentangling ecological interactions from environmental impacts on growth rates, is key to developing synthetic communities that can provide the sensory benefits of natural fermentation while lowering the risk of stuck ferments. Here, we co-culture all pairwise combinations of five commonly isolated wine-fermenting yeasts and show that competitive outcomes are a strong function of ethanol concentration, with frequency-dependent bistable interactions common at low alcohol and an increasingly transitive competitive hierarchy developing as alcohol increases. We also show that pairwise outcomes are predictive of five-species community outcomes, and that frequency dependence in pairwise interactions propagates to alternative states in the full community, highlighting the importance of species abundance as well as composition. We also observe that monoculture growth rates are only weakly predictive of competitive success, highlighting the need to incorporate ecological interactions when designing synthetic fermenting communities. Nature Publishing Group UK 2023-09-13 /pmc/articles/PMC10499898/ /pubmed/37704781 http://dx.doi.org/10.1038/s42003-023-05284-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Lax, Simon
Gore, Jeff
Strong ethanol- and frequency-dependent ecological interactions in a community of wine-fermenting yeasts
title Strong ethanol- and frequency-dependent ecological interactions in a community of wine-fermenting yeasts
title_full Strong ethanol- and frequency-dependent ecological interactions in a community of wine-fermenting yeasts
title_fullStr Strong ethanol- and frequency-dependent ecological interactions in a community of wine-fermenting yeasts
title_full_unstemmed Strong ethanol- and frequency-dependent ecological interactions in a community of wine-fermenting yeasts
title_short Strong ethanol- and frequency-dependent ecological interactions in a community of wine-fermenting yeasts
title_sort strong ethanol- and frequency-dependent ecological interactions in a community of wine-fermenting yeasts
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10499898/
https://www.ncbi.nlm.nih.gov/pubmed/37704781
http://dx.doi.org/10.1038/s42003-023-05284-1
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