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.

A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts

“…; Hagman and Piskur ; Williams et al. ). 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.…”

“…; Williams et al. ). 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 ., ): Where N t is final cell density (CFU/ml), N 0 is initial cell density (CFU/ml) and t is time in hours. Fermentation time 60 h was used to estimate the intrinsic growth rate because it showed the lowest deviation among replicates.…”

“…S. 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, ). 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, ), as well as higher levels of heat and CO 2 , can be harmful or less tolerated by their competitors (Piskur and Langkjaer, ; Piškur et al ., ; Conant and Wolfe, ; Merico et al ., ; Hagman et al ., ; Williams et al ., ). Also, nitrogen source consumption and biomass production are more efficient in S. cerevisiae (Monteiro and Bisson, ; Andorrà et al ., ).…”

Natural fruits, flowers, honey, and honeybees harborHelicobacter pylori‐positive yeasts

“…In our previous studies, it was demonstrated that vacuole of Candida species which is the storage site for plenty of nutrients 7 could serve as a niche for H. pylori, outside the human stomach. 12 Yeasts have been exploited by humans since ancient times when fermentation was the primary method to prepare and preserve foods. [8][9][10][11] Yeasts are unicellular fungi which prefer nutrient-rich environments, exhibit rapid growth and multiplication in high concentrations of simple sugars, and exhibit remarkable metabolic diversity.…”