Genome Diversity and Evolution in the Budding Yeasts (Saccharomycotina)

Abstract

Considerable progress in our understanding of yeast genomes and their evolution has been made over the last decade with the sequencing, analysis, and comparisons of numerous species, strains, or isolates of diverse origins. The role played by yeasts in natural environments as well as in artificial manufactures, combined with the importance of some species as model experimental systems sustained this effort. At the same time, their enormous evolutionary diversity (there are yeast species in every subphylum of Dikarya) sparked curiosity but necessitated further efforts to obtain appropriate reference genomes. Today, yeast genomes have been very informative about basic mechanisms of evolution, speciation, hybridization, domestication, as well as about the molecular machineries underlying them. They are also irreplaceable to investigate in detail the complex relationship between genotypes and phenotypes with both theoretical and practical implications. This review examines these questions at two distinct levels offered by the broad evolutionary range of yeasts: inside the best-studied Saccharomyces species complex, and across the entire and diversified subphylum of Saccharomycotina. While obviously revealing evolutionary histories at different scales, data converge to a remarkably coherent picture in which one can estimate the relative importance of intrinsic genome dynamics, including gene birth and loss, vs. horizontal genetic accidents in the making of populations. The facility with which novel yeast genomes can now be studied, combined with the already numerous available reference genomes, offer privileged perspectives to further examine these fundamental biological questions using yeasts both as eukaryotic models and as fungi of practical importance.

Tempo and Mode of Genome Evolution in the Budding Yeast Subphylum

“…The observed pattern of widespread metabolic trait and gene losses complements the well-established losses or reductions of several flagship eukaryotic genomic and molecular features in many budding yeasts, such as introns, the molecular machinery for RNA interference, and H3K9me2/3 heterochromatin (Dujon and Louis, 2017). Evolution by loss is well documented for parasitic and symbiotic lineages (Dujon et al, 2004; Katinka et al, 2001; Spanu et al, 2010; Vogel and Moran, 2013; Wolfe et al, 1992) and in the aftermath of the whole genome duplication events where most second copies are lost (Soltis et al, 2015;…”

“…The new phylogeny divides the subphylum into 12 major clades (Figure 2), at least two and up to eight more than previously recognized (Dujon and Louis, 2017; Hittinger et al, 2015; Kurtzman and Boekhout, 2017; Kurtzman et al, 2011; Shen et al, 2016a). Several families are now well circumscribed (e.g., Pichiaceae), while other families are not reciprocally monophyletic (e.g., Dipodascaceae/Trichomonascaceae), leading us to consider them as major clades comprised of multiple known families.…”

“…This diverse group, whose genetic diversity is on par with the plant and animal lineages (Figure 1), includes the baker’s yeast and premier eukaryotic model system Saccharomyces cerevisiae (Peter et al, 2018), the common human commensal and opportunistic pathogen Candida albicans, and over 1,000 other known species with more continuing to be discovered (Dujon and Louis, 2017; Hittinger et al, 2015; Kurtzman et al, 2011). …”

Alpaca: a kmer-based approach for investigating mosaic structures in microbial genomes

“…The resulting genome may thus be mosaic, meaning that different genomic segments may possess different evolutionary origins (Martin, 1999). Genome hybridization-the joining of two or more genomes from different strains/species-can also lead to mosaic structures due to recombination of homologous segments followed by selection of those segments with fitness advantages (Dujon and Louis, 2017). As such, the genome of an individual microbe may be the result of a rich history of genetic adaptations after coming in contact with different populations (Martin, 1999;Ochman et al, 2000;Rainieri et al, 2006;Dujon and Louis, 2017).…”

Saccharomyces cerevisiaestrain YH166: a novel wild yeast for the production of tropical fruit sensory attributes in fermented beverages

“…These organisms are ubiquitous in such applications due to their naturally high levels of tolerance to ethanol (EtOH), low pH, osmotic stress, and anaerobic conditions (2-4). Of the eight species in the genus Saccharomyces ( S. arboricola , S. cerevisiae , S. eubayanus , S. jurei , S. kudriavzevii , S. mikatae , S. paradoxus , and S. uvarum ) (5), S. cerevisiae is most commonly found in traditionally fermented beverages and is used industrially for beverage fermentation and bioethanol production (1,6). Indeed, S. cerevisiae is used for ale and wine production worldwide.…”