Evolution of ecological dominance of yeast species in high-sugar environments

Abstract

In budding yeasts, fermentation in the presence of oxygen evolved around the time of a whole genome duplication (WGD) and is thought to confer dominance in high-sugar environments because ethanol is toxic to many species. While there are many fermentative yeast species, only Saccharomyces cerevisiae consistently dominates wine fermentations. In this study, we use co-culture experiments and intrinsic growth rate assays to examine the relative fitness of non-WGD and WGD yeast species across environments to assess when S. cerevisiae's ability to dominate high-sugar environments arose. We show that S. cerevisiae dominates nearly all other non-WGD and WGD species except for its sibling species S. paradoxus in both grape juice and a high-sugar rich medium. Of the species we tested, S. cerevisiae and S. paradoxus have evolved the highest ethanol tolerance and intrinsic growth rate in grape juice. However, the ability of S. cerevisiae and S. paradoxus to dominate certain species depends on the temperature and the type of high-sugar environment. Our results indicate that dominance of high-sugar environments evolved much more recently than the WGD, most likely just prior to or during the differentiation of Saccharomyces species, and that evolution of multiple traits contributes to S. cerevisiae's ability to dominate wine fermentations.

Impact of Sucrose Addition on the Physiochemical Properties and Volatile Compounds of “Shuangyou” Red Wines

“…In addition, during fermentation, the highest sugar consumption was observed in the sample with the highest amount (100 g/L) of added sucrose (Figure 2(a) and Table 1). This indicates that the fermentative lifestyle could exhibit a growth advantage in sugar-rich environments due to a higher rate of sugar conversion and energy production [35]. Journal of Food Quality …”

A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts

“…A second important assumption, particularly for diversification analysis, is that taxon sampling is complete or at-least complete, and a random sample of the known diversity. This limitation is inherent to the phylogeny being used, which for the our case seems to be the most complete (studies based on Kurtzman and Robnett phylogeny: Hall et al 2005;Hagman et al 2013Hagman et al , 2014Dashko et al 2014;Hagman and Piskur 2015;Williams et al 2015). Although we don't have reasons to think that this phylogeny is biased or unrepresentative, the fact that there exist more than thousands described yeasts species (see Kurtzman et al 2011) warrants further confirmatory studies, with new, larger phylogenies.…”

“…According to a number of authors, the appearance of fruits coincided with the appareance of fermentative yeasts (especially Saccharomyces), which has supported the hypothesis of novel ecological niches provided by fruits and simple sugars (Hagman et al 2013;Dashko et al 2014;Williams et al 2015). These authors suggested that fermentative capacity represents an ecological innovation that triggered an adaptive radiation.…”

Dominance of wine Saccharomyces cerevisiae strains over S. kudriavzevii in industrial fermentation competitions is related to an acceleration of nutrient uptake and utilization

“…To measure fitness, we calculated the intrinsic growth rate (r) using the exponential growth equation (Williams et al, 2015):…”

“…cerevisiae yeasts are characterized by their high capability to ferment simple sugars into ethanol even in the presence of oxygen, known as Crabtree effect (Crabtree, 1928). Although, alcohol fermentation is energetically much less efficient than aerobic respiration, it provides with a selective advantage to these yeasts to outcompete other microorganisms: sugar resources are consumed faster and the ethanol produced during fermentation (Goddard, 2008), as well as higher levels of heat and CO 2 , can be harmful or less tolerated by their competitors (Piskur and Langkjaer, 2004;Piškur et al, 2006;Conant and Wolfe, 2007;Merico et al, 2007;Hagman et al, 2013;Williams et al, 2015). Also, nitrogen source consumption and biomass production are more efficient in S. cerevisiae (Monteiro and Bisson, 1991;Andorrà et al, 2012).…”