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Yeast “Make-Accumulate-Consume” Life Strategy Evolved as a Multi-Step Process That Predates the Whole Genome Duplication
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When fruits ripen, microbial communities start a fierce competition for the freely available fruit sugars. Three yeast lineages, including baker's yeast Saccharomyces cerevisiae, have independently developed the metabolic activity to convert simple sugars into ethanol even under fully aerobic conditions. This fermentation capacity, named Crabtree effect, reduces the cell-biomass production but provides in nature a tool to out-compete other microorganisms. Here, we analyzed over forty Saccharomycetaceae yeasts, covering over 200 million years of the evolutionary history, for their carbon metabolism. The experiments were done under strictly controlled and uniform conditions, which has not been done before. We show that the origin of Crabtree effect in Saccharomycetaceae predates the whole genome duplication and became a settled metabolic trait after the split of the S. cerevisiae and Kluyveromyces lineages, and coincided with the origin of modern fruit bearing plants. Our results suggest that ethanol fermentation evolved progressively, involving several successive molecular events that have gradually remodeled the yeast carbon metabolism. While some of the final evolutionary events, like gene duplications of glucose transporters and glycolytic enzymes, have been deduced, the earliest molecular events initiating Crabtree effect are still to be determined.
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“many aspects of its energy metabolism are relatively recent evolutionary adaptations to the predominantly fermentative lifestyle and are not typical of other yeast lineages”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Hagman et al. 2013
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“S. cerevisiae belongs to yeasts exhibiting the Crabtree effect—preference for fermentative energy production in high glucose concentration even in the presence of oxygen (Hagman et al. 2013; Pfeiffer and Morley 2014; Williams et al. 2015; Nespolo et al. 2020).”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Hagman et al. 2013
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Metadata
- Authors
- Hagman, A., Säll, T., Compagno, C., & Piskur, J.
- Affiliations
- Lund University (SE)
- University of Milan (IT)
- Corresponding author
- Hagman, Arne
- Säll, Torbjörn
- Compagno, Concetta
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-07-15
- Volume
- 8
- Issue
- 7
- Pages
- e68734
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3711898
- OpenAlex
- W2158180844
- Cited by
- 219
- References
- 31
- Citations by year
- 2026: 10 · 2025: 15 · 2024: 12 · 2023: 20 · 2022: 17 · 2021: 29 · 2020: 12 · 2019: 21 · 2018: 17 · 2017: 16 · 2016: 17 · 2015: 15 · 2014: 18
- FWCI
- 7.47
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Lund University Publications (Lund University) (submittedVersion, other-oa)
- Funders
- Vetenskapsrådet
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Immunology and Microbiology › Microbiology › Yeasts and Rust Fungi Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Keywords
- Crabtree effect, alcoholic fermentation, Saccharomyces cerevisiae, Saccharomycetaceae, yeast evolution, whole-genome duplication, carbon metabolism, glucose transporters, glycolytic enzymes, gene duplication, fruit ripening, microbial competition, fruit-bearing plants, aerobic fermentation
- MeSH terms
- Carbon, Saccharomycetales, Fermentation, Glucose, Genome, Fungal, Evolution, Molecular
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