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Saccharomyces cerevisiae - an alcohol producer tuned to perfection

In order to thrive in a fermentation environment, Saccharomyces spp. in general (and S. cerevisiae in particular) possess several phenotypic features that make them the ultimate fermentation specialists they are today. These features arose gradually during evolution, both inside and outside manmade fermentation environments.

Natural selection shaped the Saccharomyces genome

One of the most striking attributes of Saccharomyces spp. is their perfect adaptation to sugar-rich, oxygen-limited environments. It was hypothesized that the emergence of fruit-bearing plants (a new niche that provided a rich, but highly competitive source of ready-to-use sugars) approximately 80-150 million years ago triggered the selection of a cascade of specific genetic adaptations, all targeted towards colonization of these new niches. Therefore, it seems obvious that these adaptations happened by natural selection, and no man-mediated (artificial) selection was involved.

One of the most striking examples is the emergence of the so-called ‘Crabtree effect' in Saccharomyces. Crabtree-positive yeasts show a metabolism in which glucose (above a certain threshold concentration) represses respiration, so that even when oxygen is still available, cells will favour fermentation. This persistent fermentative behaviour has several advantages over respiration. First, fermentation enables a higher carbon flux and faster production of energy. Second, the main end- product of a fermentative metabolism is ethanol, which can serve as an effective antimicrobial agent, to which Saccharomyces itself is highly tolerant. Therefore, the Crabtree effect fits a make-accu- mulate-consume strategy, an ecological strategy in which ethanol is first produced and accumulated to high concentrations to inhibit the growth of other microbes and later consumed again when all fermentable sugars have been converted (Thomson et al., 2005). Apart from the Crabtree effect, there are several other physiological features that provide Saccharomyces spp. with a competitive advantage in fermentation-like environments (e.g. rotting fruit). They have evolved a high tolerance to several environmental stresses (such as high temperatures and a high concentration of osmolytes), a very high glycolytic flux, and the ability to grow in both aerobic and anaerobic conditions (Conant and Wolfe, 2007; Goddard, 2008; Piskur et al., 2006). It is interesting to note that these individual properties are also present in various other yeasts, but they are only uniquely combined in a few species, including S. cerevisiae and its closest relatives, providing a strong competitive advantage over other wild yeasts (and bacteria) in many fermentation environments (Piskur et al., 2006).

While most of these properties are now common knowledge, the underlying genetics were only investigated recently. While many questions remain unsolved, these studies led to the first hints towards the evolutionary pathways Saccharomyces spp. went through in response to these newly emerged niches. For example, it was shown that the duplication of several key genes, such as those encoding alcohol dehydrogenase (Hagman et al., 2013; Thomson et al., 2005), hexose transporters (Lin and Li, 2011), and enzymes linked to glycolysis (Conant and Wolfe, 2007), as well as global rewiring of the transcriptional network after whole-genome duplication (Ihmels et al., 2005), played a major role in the evolution of Saccharomyces.

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