Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity

Abstract

The budding yeast, Saccharomyces cerevisiae, is a leading system in genetics, genomics and molecular biology and is becoming a powerful tool to illuminate ecological and evolutionary principles. However, little is known of the ecology and population structure of this species in nature. Here, we present a field survey of this yeast at an unprecedented scale and have performed population genetics analysis of Chinese wild isolates with different ecological and geographical origins. We also included a set of worldwide isolates that represent the maximum genetic variation of S. cerevisiae documented so far. We clearly show that S. cerevisiae is a ubiquitous species in nature, occurring in highly diversified substrates from human-associated environments as well as habitats remote from human activity. Chinese isolates of S. cerevisiae exhibited strong population structure with nearly double the combined genetic variation of isolates from the rest of the world. We identified eight new distinct wild lineages (CHN I-VIII) from a set of 99 characterized Chinese isolates. Isolates from primeval forests occur in ancient and significantly diverged basal lineages, while those from human-associated environments generally cluster in less differentiated domestic or mosaic groups. Basal lineages from primeval forests are usually inbred, exhibit lineage-specific karyotypes and are partially reproductively isolated. Our results suggest that greatly diverged populations of wild S. cerevisiae exist independently of and predate domesticated isolates. We find that China harbours a reservoir of natural genetic variation of S. cerevisiae and perhaps gives an indication of the origin of the species.

Mitochondrial-Nuclear Epistasis Contributes to Phenotypic Variation and Coadaptation in Natural Isolates of Saccharomyces cerevisiae

“…Genetic diversity and global population structures of S. cerevisiae yeasts have been revealed through numerous large-scale sequencing projects Wang et al 2012;Cromie et al 2013). We did not find evidence that the genetic distances between the original strains correlated with their phenotypes ( Figure S4).…”

“…With next-generation sequencing technologies, S. cerevisiae yeasts are now being thrust into the limelight for population genetics and phenomics. As such, population structures for wild yeasts are better understood Wang et al 2012;Cromie et al 2013;Hittinger 2013;Skelly et al 2013) and an increasing number of laboratory-friendly isolates representing the genetic diversity of yeasts are now available (Cubillos et al 2009;Louvel et al 2014).…”

Effect of Domestication on the Spread of the [PIN+] Prion inSaccharomyces cerevisiae

“…were detected in the ancestral clade, consisting of isolates sampled from soil, insects, fermented food, grapes, and African wine strains. The ancestral clade was the oldest lineage, showing the most similarity to S. paradoxus, a yeast that exists worldwide in natural environments, but has little or no association with humans (Sniegowski et al 2002;Fay and Benavides 2005;Koufopanou et al 2006;Sampaio and Goncalves 2008;Wang et al 2012). Like ancient, wild strains of S. cerevisiae sampled in primeval forests of China (Wang et al 2012), isolates from the ancestral clade showed the highest levels of inbreeding and reproductive isolation.…”

“…Additionally, flocculation, characterized by increased cell-cell adhesion resulting in aggregates of vegetative cells, is often observed when sugars are depleted from the media (Guo et al 2000). Enhanced cellular aggregation provides protection in harsh environments (Bruckner and Mosch 2011), and flocculent yeast strains are often utilized in beer fermentation and other industrialized settings (Verstrepen and Klis 2006).The yeast S. cerevisiae has been isolated globally from a variety of natural substrates (fruit, tree bark, soil) (Sniegowski et al 2002;Wang et al 2012) and from environments closely associated with human activity (breweries, bakeries, vineyards) (Legras et al 2007). We refer to strains isolated and adapted (or bred) for human use as domesticated strains.…”

“…The yeast S. cerevisiae has been isolated globally from a variety of natural substrates (fruit, tree bark, soil) (Sniegowski et al 2002;Wang et al 2012) and from environments closely associated with human activity (breweries, bakeries, vineyards) (Legras et al 2007). We refer to strains isolated and adapted (or bred) for human use as domesticated strains.…”