Genomics and Evolution Studies of Dekkera bruxellensis, a Wine-Spoilage Yeast

Abstract: Yeasts are unicellular fungi exhibiting a huge diversity of life styles and physiologies and their evolutionary span exceeds the one between mammals and unchordates. The recent advances in genome sequencing and comparative genomics accelerated genomic, evolutionary and physiological studies of yeasts, making them a very promising model to study eukaryotic cell, and also deepened our understanding of the molecular background of yeasts physiologies. The most extensively studied yeasts species Saccharomyces cerevisiae, and its close relatives, exhibit several unique physiological characteristics like (i) ethanol production under aerobic conditions (Crabtree effect), (ii) ability to grow in almost total absence of oxygen and (iii) the ability to generate respiratory deficient (petite) mutants. These traits form a frame for the development of the so-called “make-accumulate-consume” strategy, which helps Saccharomyces yeasts to out-compete other microbes when a lot of sugars are present in the environment. Several molecular events contributed to the above mentioned characteristics of modern yeasts, among them the whole genome duplication (WGD), rewiring of the expression network, horizontal gene transfer and the duplication of the gene coding for alcohol dehydrogenase. However, even though S. cerevisiae reached perfection in efficient ethanol production and ability to grow anaerobically, apparently it is not unique among yeasts. Dekkera bruxellensis that diverged from S. cerevisiae more than 200 mya is also an efficient ethanol producer and can grow anaerobically. We show that the same molecular mechanism was involved independently in the development of the “make-accumulate-consume” strategy in both lineages. In other words, both yeast lineages followed a parallel evolutionary path to reach the same phenotype. A relative of D. bruxellensis, the human pathogen Candida albicans that belongs to the pre-WGD group is unable of efficient aerobic ethanol production and cannot grow in anaerobiosis. It grows rapidly in aerobic conditions, using the carbon source on biomass production and not on alcohol synthesis. We prove that C. albicans exhibits the Crabtree negative phenotype and is obligate aerobe, two traits characteristic for the progenitor of the modern yeasts.