Fermentative lifestyle in yeasts belonging to the Saccharomyces complex

Abstract

The concentration of oxygen in the environment is one of the most important factors that regulate energy conversion in living cells. Organisms have developed multiple processes to optimize the utilization of oxygen when its availability is reduced. According to the role of oxygen in their metabolism, yeasts can be classified as: (a) obligate aerobes, displaying an exclusively respiratory metabolism; (b) facultative fermentatives, displaying both respiratory and fermentative metabolism; and (c) obligate fermentatives. The ability of yeasts to grow in very oxygen-limited conditions is strictly dependent on the ability to perform alcoholic fermentation, allowing reoxidation of NADH generated during glycolysis. In Saccharomyces cerevisiae, fermentation predominates over respiration when glucose concentrations are high, even under aerobic conditions. Depending on this characteristic, yeasts are classified as Crabtree-positive or Crabtreenegative. Thus, in Crabtree-positive yeasts, such as S. cerevisiae, NADH is mainly oxidized in glucose- The yeast Saccharomyces cerevisiae is characterized by its ability to: (a) degrade glucose or fructose to ethanol, even in the presence of oxygen (Crabtree effect); (b) grow in the absence of oxygen; and (c) generate respiratory-deficient mitochondrial mutants, so-called petites. How unique are these properties among yeasts in the Saccharomyces clade, and what is their origin? Recent progress in genome sequencing has elucidated the phylogenetic relationships among yeasts in the Saccharomyces complex, providing a framework for the understanding of the evolutionary history of several modern traits. In this study, we analyzed over 40 yeasts that reflect over 150 million years of evolutionary history for their ability to ferment, grow in the absence of oxygen, and generate petites. A great majority of isolates exhibited good fermentation ability, suggesting that this trait could already be an intrinsic property of the progenitor yeast. We found that lineages that underwent the whole-genome duplication, in general, exhibit a fermentative lifestyle, the Crabtree effect, and the ability to grow without oxygen, and can generate stable petite mutants. Some of the pre-genome duplication lineages also exhibit some of these traits, but a majority of the tested species are petite-negative, and show a reduced Crabtree effect and a reduced ability to grow in the absence of oxygen. It could be that the ability to accumulate ethanol in the presence of oxygen, a gradual independence from oxygen and ⁄ or the ability to generate petites were developed later in several lineages. However, these traits have been combined and developed to perfection only in the lineage that underwent the whole-genome duplication and led to the modern Saccharomyces cerevisiae yeast.Abbreviation EtBr, ethidium bromide.

QUANTIFYING THE COMPLEXITIES OFSACCHAROMYCES CEREVISIAE'S ECOSYSTEM ENGINEERING VIA FERMENTATION

“…The rise in temperature and ethanol as a result of the Crabtree effect trait was operated on by natural selection because it increased S. cerevisiae's fitness. It seems this is an adaptation that only S. cerevisiae possesses in this particular community: none of the other species were able to ferment the grape juice to completion (M. R. Goddard, unpublished data), and their lineages are all positioned before the yeast whole-genome duplication event and therefore demonstrate either an absence or significantly diminished Crabtree effect (Merico et al 2007). These data correlate with the reports that S. cerevisiae dominates more rapidly in traditional ferments with higher temperature (Heard and Fleet 1988), and observations that higher temperature ferments experience less problems from non-Saccharomyces yeasts.…”

Influence of Oxygen on Alcoholic Fermentation by a Wine Strain ofTorulaspora delbrueckii: Kinetics and Carbon Mass Balance

“…According to the literature, this non-Saccharomyces yeast is classified among the Crabtree-negative 18) or Crabtree-positive organisms, but with less sensitivity than Saccharomyces according to Alves-Araujo et al 12) and Merico et al 17) These authors explain that even under limited oxygen conditions, the yield of biomass production of T. delbrueckii remains higher than that of S. cerevisiae due to the greater proportion of carbon that can flow in the respiratory metabolism. Our results are in accord with these last authors.…”

“…In some cases, it has been reported that T. delbrueckii does not grow under anaerobic conditions. [14][15][16] In a variety of studies, it is also classified as a Crabtree-positive 12,17) or a Crabtreenegative species. 18) The objective of this study was to test and quantify the influence of oxygenation on the metabolism of one T. delbrueckii strain selected for wine production.…”

The tragedy of the commons in microbial populations: insights from theoretical, comparative and experimental studies

“…Plotted points in panel c show the rate and yield of glucose metabolism in exponentially growing cultures of yeast species. Data are taken from Merico et al (2007). Species that ferment glucose to produce ethanol are shown with open symbols and those species that do not produce ethanol are shown with filled symbols.…”