Why, when, and how did yeast evolve alcoholic fermentation?

Abstract

The origin of modern fruits brought to microbial communities an abundant source of rich food based on simple sugars. Yeasts, especially Saccharomyces cerevisiae, usually become the predominant group in these niches. One of the most prominent and unique features and likely a winning trait of these yeasts is their ability to rapidly convert sugars to ethanol at both anaerobic and aerobic conditions. Why, when, and how did yeasts remodel their carbon metabolism to be able to accumulate ethanol under aerobic conditions and at the expense of decreasing biomass production? We hereby review the recent data on the carbon metabolism in Saccharomycetaceae species and attempt to reconstruct the ancient environment, which could promote the evolution of alcoholic fermentation. We speculate that the first step toward the so-called fermentative lifestyle was the exploration of anaerobic niches resulting in an increased metabolic capacity to degrade sugar to ethanol. The strengthened glycolytic flow had in parallel a beneficial effect on the microbial competition outcome and later evolved as a "new" tool promoting the yeast competition ability under aerobic conditions. The basic aerobic alcoholic fermentation ability was subsequently "upgraded" in several lineages by evolving additional regulatory steps, such as glucose repression in the S. cerevisiae clade, to achieve a more precise metabolic control.

Keywords: alcoholic fermentation; carbon metabolism; evolution; life strategy; yeast.

Figure 1

Phylogenetic relationship among some yeasts. Note that some of the shown yeast lineages separated from each other many million years ago and have therefore accumulated several molecular and physiological changes regarding their carbon metabolism. However, during the evolutionary history, there have also been parallel events. Apparently, at least three lineages, Saccharomyces, Dekkera, and Schizosaccharomyces, have evolved (1) the ability to ferment in the presence of oxygen and (2) to proliferate under anaerobic conditions. This figure was adopted from Compagno et al. (2014).

Figure 2

The Saccharomycetaceae family covers over 200 million years of the yeast evolutionary history and includes six post-whole-genome duplication (post-WGD) genera, Saccharomyces, Kazachstania, Naumovia, Nakaseomyces, Tetrapisispora, and Vanderwaltozyma; and six non-WGD genera, Zygosaccharomyces, Zygotorulaspora, Torulaspora, Lachancea, Kluyveromyces, and Eremothecium. Hereby, we show a rough phylogenetic relationship among these genera. Two evolutionary events are shown, WGD, which took place app. 100 million years ago and the loss of Respiratory Complex I (which took place app. 150 million years ago). This figure was adopted from Hagman et al. (2013).

Figure 3

Crabtree effect results in lower biomass production because a fraction of sugar is converted into ethanol. This means that more glucose has to be consumed to achieve the same yield of cells if comparing with Crabtree-negative yeasts. Because only a fraction of sugar is used for the biomass and energy production, this could theoretically result in lower growth rate in Crabtree-positive yeasts and these could then simply be out-competed by Crabtree-negative yeasts and other microorganisms. However, ethanol could be used as a tool to slow down and control the proliferation of other competitive microorganisms.