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

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.

Analysis of the yeast short‐term Crabtree effect and its origin

“…It has previously been shown that Crabtree-positive yeast species show high glucose consumption rates 14. Here we show that the glucose uptake rates and ethanol production rates for all fermenting yeasts are equal to or higher than K. marxianus , which is the SCN yeast with the highest initial glucose uptake rate in our experiments.…”

“…K. lactis is short-term Crabtree-positive (present results), but long-term Crabtree-negative (Table1 and Fig. S7) 14. Other investigated yeast species that diverged from the rest of the Saccharomyces lineage prior to, or at approximately the same time as K. lactis , such as P. pastoris , D. vanrijiae , E. coryli and K. marxianus , are both short- and long-term Crabtree-negative 14.…”

“…Although the number of studied yeasts in our paper is only ten, we speculate that the time of origin of the short-term Crabtree effect and the time of origin of the long-term Crabtree effect are very close to each other and may even overlap, coinciding with the horizontal transfer of URA1 gene (encoding a bacterial ‘anaerobic’ DHODase) and the ability to proliferate anaerobically (Fig. S7) 14,17. Furthermore, this study has generated a large collection of data that may be used to develop a model to elucidate the mechanisms behind the observed results and help to reconstruct the evolutionary pathways leading to the modern traits in extant yeasts.…”

“…S7) 14. Other investigated yeast species that diverged from the rest of the Saccharomyces lineage prior to, or at approximately the same time as K. lactis , such as P. pastoris , D. vanrijiae , E. coryli and K. marxianus , are both short- and long-term Crabtree-negative 14. Although the number of studied yeasts in our paper is only ten, we speculate that the time of origin of the short-term Crabtree effect and the time of origin of the long-term Crabtree effect are very close to each other and may even overlap, coinciding with the horizontal transfer of URA1 gene (encoding a bacterial ‘anaerobic’ DHODase) and the ability to proliferate anaerobically (Fig.…”

Microbial and Chemical Diversity of Traditional Non-Cereal Based Alcoholic Beverages of Sub-Saharan Africa

“…This suggests that Saccharomyces yeasts are the most dominant alcoholic fermentation microorganisms [75][76][77]. Even in the presence of oxygen, S. cerevisiae, is the predominant yeast species responsible for the production of ethanol [78,79]. The production of ethanol, toxic to other microbes, has been hypothesized to be a niche defense mechanism for S. cerevisiae [42].…”