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Cited by 220Fungal and yeast genetics researchYeasts and Rust Fungi StudiesMicrobial Metabolic Engineering and Bioproduction

The DOI matches its Crossref record; 30 of the 31 references it cites were found in a registry or an index.

Yeast “Make-Accumulate-Consume” Life Strategy Evolved as a Multi-Step Process That Predates the Whole Genome Duplication

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Hagman, Arne, Säll, Torbjörn, Compagno, Concetta, Piskur, Jure·2013·PLoS ONE
DOI 10.1371/journal.pone.0068734PMC PMC3711898
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Abstract

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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Figures

Figure 1 Phylogenetic relationship among yeast. A schematic phylogenetic relationship, based on the phylogenetic tree from Kurtzman and Robnett (2003) [16], covering twelve genera of Saccharomycetaceae and all employed species. Note that alternative models to explain the phylogenetic relationship between the Lachancea, Kluyveromyces and Eremothecium genera have been proposed [23] but here we follow the tree in ref. 15. Several evolutionary events, which are relevant for the modern traits, are shown. Note that the relative timing of some events, especially those which left a clear finger-print in the modern genomes (green arrows) is relatively precise, such as WGD [10], the horizontal transfer of a bacterial »anaerobic« DHODase (encoded by URA1) [19], complete rewiring of the respiration related promoters (RGE stands for Rapid Growth Elements) [3], and the loss of respiratory Complex I [9], while the timing of more complex traits (red arrows), such as the capability for anaerobic growth [12], [13] and petite positivity [13], might be less precise.
Figure 1 Phylogenetic relationship among yeast. A schematic phylogenetic relationship, based on the phylogenetic tree from Kurtzman and Robnett (2003) [16], covering twelve genera of Saccharomycetaceae and all employed species. Note that alternative models to explain the phylogenetic relationship between the Lachancea, Kluyveromyces and Eremothecium genera have been proposed [23] but here we follow the tree in ref. 15. Several evolutionary events, which are relevant for the modern traits, are shown. Note that the relative timing of some events, especially those which left a clear finger-print in the modern genomes (green arrows) is relatively precise, such as WGD [10], the horizontal transfer of a bacterial »anaerobic« DHODase (encoded by URA1) [19], complete rewiring of the respiration related promoters (RGE stands for Rapid Growth Elements) [3], and the loss of respiratory Complex I [9], while the timing of more complex traits (red arrows), such as the capability for anaerobic growth [12], [13] and petite positivity [13], might be less precise.CC BY · PubMed Central
Figure 2 Yeast growth profiles. A few examples of a representative batch culture experiment showing different capacity to produce ethanol and biomass in the presence of excess glucose and oxygen: Sac. eubayanus (A), Kaz. exiguus (B), Zto. mrakii (C), Lac. waltii (D), Klu. wickerhamii (E) and Ere. sinecaudum (F). The graphs show time dependence of yeast glucose consumption, and appearance of the fermentation products and biomass. The ethanol and biomass yields vary enormously among the six shown species, as well as among other studied yeasts (table 1), and are related to the phylogenetic position of each studied yeast species (see also figure 1).
Figure 2 Yeast growth profiles. A few examples of a representative batch culture experiment showing different capacity to produce ethanol and biomass in the presence of excess glucose and oxygen: Sac. eubayanus (A), Kaz. exiguus (B), Zto. mrakii (C), Lac. waltii (D), Klu. wickerhamii (E) and Ere. sinecaudum (F). The graphs show time dependence of yeast glucose consumption, and appearance of the fermentation products and biomass. The ethanol and biomass yields vary enormously among the six shown species, as well as among other studied yeasts (table 1), and are related to the phylogenetic position of each studied yeast species (see also figure 1).CC BY · PubMed Central
Figure 3 Yeast ethanol and biomass yield. Different yeast species were studied for their carbon metabolism: ethanol yield as g of ethanol per g of glucose (red), and biomass yield as g of biomass per g of glucose (blue). Detailed results and biological replicates are shown in table 1 but hereby either a single measurement or an average of two replicates are presented. The yeast species are presented starting with the Saccharomyces genus at the top and then following a decreasing phylogenetic relationship, following figure 1. The species related the least to S. cerevisiae are at the bottom, and the gap divides the Saccharomycotina and non-Saccharomycotina yeasts. The four groups of yeasts (1, 2, 3 and 4) used in the statistical analysis are shown. In general, the ethanol yield gradually drops and the biomass yield gradually increases with the genetic distance from the Saccharomyces yeasts (see also figure 5 A and B).
Figure 3 Yeast ethanol and biomass yield. Different yeast species were studied for their carbon metabolism: ethanol yield as g of ethanol per g of glucose (red), and biomass yield as g of biomass per g of glucose (blue). Detailed results and biological replicates are shown in table 1 but hereby either a single measurement or an average of two replicates are presented. The yeast species are presented starting with the Saccharomyces genus at the top and then following a decreasing phylogenetic relationship, following figure 1. The species related the least to S. cerevisiae are at the bottom, and the gap divides the Saccharomycotina and non-Saccharomycotina yeasts. The four groups of yeasts (1, 2, 3 and 4) used in the statistical analysis are shown. In general, the ethanol yield gradually drops and the biomass yield gradually increases with the genetic distance from the Saccharomyces yeasts (see also figure 5 A and B).CC BY · PubMed Central
Figure 4 Yeast glucose consumption, ethanol production and growth rates. Different yeast species were studied for their carbon metabolism and the results are shown as: specific glucose consumption rate (g/g h-1 amount of consumed glucose by 1 g of biomass and multiplied with the corresponding specific growth rate, shown in blue), specific ethanol production rate (g/g h-1 ethanol produced by 1 g biomass and multiplied with the corresponding specific growth rate, shown in red), and specific growth rate (per hour, shown in green). Detailed results and biological replicates are shown in table 1 but hereby either a single measurement or an average of two replicates are presented. The yeast species are presented starting with the Saccharomyces genus at the top and then following a decreasing phylogenetic relationship, according to figure 1. The species related the least to S. cerevisiae are at the bottom, and the gap divides the Saccharomycotina and non-Saccharomycotina yeasts. The four groups of yeasts (1, 2, 3 and 4) used in the statistical analysis are shown (see also figure 3). Specific glucose consumption rate decreases with the phylogenetic distance from the Saccharomyces genus, indicating that Crabtree negative yeasts have only a moderate rate, while Crabtree positive have faster glucose consumption rate. On the other hand, the growth rate (in green) is very similar among all Saccharomycotina yeasts (see also figure 5 C and D).
Figure 4 Yeast glucose consumption, ethanol production and growth rates. Different yeast species were studied for their carbon metabolism and the results are shown as: specific glucose consumption rate (g/g h-1 amount of consumed glucose by 1 g of biomass and multiplied with the corresponding specific growth rate, shown in blue), specific ethanol production rate (g/g h-1 ethanol produced by 1 g biomass and multiplied with the corresponding specific growth rate, shown in red), and specific growth rate (per hour, shown in green). Detailed results and biological replicates are shown in table 1 but hereby either a single measurement or an average of two replicates are presented. The yeast species are presented starting with the Saccharomyces genus at the top and then following a decreasing phylogenetic relationship, according to figure 1. The species related the least to S. cerevisiae are at the bottom, and the gap divides the Saccharomycotina and non-Saccharomycotina yeasts. The four groups of yeasts (1, 2, 3 and 4) used in the statistical analysis are shown (see also figure 3). Specific glucose consumption rate decreases with the phylogenetic distance from the Saccharomyces genus, indicating that Crabtree negative yeasts have only a moderate rate, while Crabtree positive have faster glucose consumption rate. On the other hand, the growth rate (in green) is very similar among all Saccharomycotina yeasts (see also figure 5 C and D).CC BY · PubMed Central
Figure 5 Statistical analysis of the fermentation parameters. Yeasts have been grouped into the following groups: Group 1 included all tested species belonging to Eremothecium and Kluyveromyces, group 2 all strains of the Lachancea, Torulaspora and Zygotorulaspora genera, group 3 contain the Vandervaltozyma and Tetrapisispora, and group 4 all species belonging to the Saccharomyces, Kazachstania, Naumovozyma and Nakaseomyces genera. The group mean values on four parameters: ethanol yield (A), biomass yield (B), glucose consumption rate (C) and growth rate (D) are illustrated. All error bars in the figure cover a 95% confidence interval for each group. Group 3 appears to be an intermediate between group 2 and 4 for all parameters except growth rate. Hence, no significant difference in growth rates among groups can be observed. These results are also supported by statistical analysis of variance and pairwise t-test (table 2).
Figure 5 Statistical analysis of the fermentation parameters. Yeasts have been grouped into the following groups: Group 1 included all tested species belonging to Eremothecium and Kluyveromyces, group 2 all strains of the Lachancea, Torulaspora and Zygotorulaspora genera, group 3 contain the Vandervaltozyma and Tetrapisispora, and group 4 all species belonging to the Saccharomyces, Kazachstania, Naumovozyma and Nakaseomyces genera. The group mean values on four parameters: ethanol yield (A), biomass yield (B), glucose consumption rate (C) and growth rate (D) are illustrated. All error bars in the figure cover a 95% confidence interval for each group. Group 3 appears to be an intermediate between group 2 and 4 for all parameters except growth rate. Hence, no significant difference in growth rates among groups can be observed. These results are also supported by statistical analysis of variance and pairwise t-test (table 2).CC BY · PubMed Central

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Research works printed but not linked: 1

  1. Kurtzman CP, Fell JW, Boekhout T (2011) The Yeasts, a Taxanomic Study. London: Elsevier. 2080 p.

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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
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2013-07-15
Volume
8
Issue
7
Pages
e68734
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0068734
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
Licence
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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