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Genome introgressions drive evolution across the animal 1 , plant 2 and fungal 3 kingdoms. Introgressions initiate from archaic admixtures followed by repeated backcrossing to one parental species. However, how introgressions arise in reproductively isolated species, such as yeast 4 , has remained unclear. Here we identify a clonal descendant of the ancestral yeast hybrid that founded the extant Saccharomyces cerevisiae Alpechin lineage 5 , which carries abundant Saccharomyces paradoxus introgressions. We show that this clonal descendant, hereafter defined as a ‘living ancestor’, retained the ancestral genome structure of the first-generation hybrid with contiguous S. cerevisiae and S. paradoxus subgenomes. The ancestral first-generation hybrid underwent catastrophic genomic instability through more than a hundred mitotic recombination events, mainly manifesting as homozygous genome blocks generated by loss of heterozygosity. These homozygous sequence blocks rescue hybrid fertility by restoring meiotic recombination and are the direct origins of the introgressions present in the Alpechin lineage. We suggest a plausible route for introgression evolution through the reconstruction of extinct stages and propose that genome instability allows hybrids to overcome reproductive isolation and enables introgressions to emerge. A yeast clonal descendant of an ancient hybridization event is identified and sheds light on the early evolution of the Saccharomyces cerevisiae Alpechin lineage and its abundant Saccharomyces paradoxus introgressions.

Novel protein-coding genes can arise either from pre-existing genes or de novo ; here it is shown that functional genes emerge de novo through transitory proto-genes generated by widespread translational activity in non-genic sequences. New genes from unlikely beginnings De novo gene birth has occurred in many lineages during evolution, but how functional protein-coding genes emerge in non-functional sequences — rather than through gene rearrangement — remains unresolved. These authors observe in the yeast Saccharomyces cerevisiae that hundreds of species-specific non-genic transcripts are differentially regulated upon stress. These previously overlooked translation events seem to act as a reservoir of adaptive potential, in the form of open reading frames that occupy an evolutionary continuum ranging from non-genic sequences to genes. On the basis of their genome-wide observations, the authors suggest that de novo gene birth from the proto-gene reservoir may be more prevalent than sporadic gene duplication. Novel protein-coding genes can arise either through re-organization of pre-existing genes or de novo 1 , 2 . Processes involving re-organization of pre-existing genes, notably after gene duplication, have been extensively described 1 , 2 . In contrast, de novo gene birth remains poorly understood, mainly because translation of sequences devoid of genes, or ‘non-genic’ sequences, is expected to produce insignificant polypeptides rather than proteins with specific biological functions 1 , 3 , 4 , 5 , 6 . Here we formalize an evolutionary model according to which functional genes evolve de novo through transitory proto-genes 4 generated by widespread translational activity in non-genic sequences. Testing this model at the genome scale in Saccharomyces cerevisiae , we detect translation of hundreds of short species-specific open reading frames (ORFs) located in non-genic sequences. These translation events seem to provide adaptive potential 7 , as suggested by their differential regulation upon stress and by signatures of retention by natural selection. In line with our model, we establish that S. cerevisiae ORFs can be placed within an evolutionary continuum ranging from non-genic sequences to genes. We identify ∼1,900 candidate proto-genes among S. cerevisiae ORFs and find that de novo gene birth from such a reservoir may be more prevalent than sporadic gene duplication. Our work illustrates that evolution exploits seemingly dispensable sequences to generate adaptive functional innovation.

From yeasts to humans, introgressive hybridization significantly influences the evolutionary history of living organisms by introducing new genetic diversity. Strains of Saccharomyces cerevisiae worldwide exhibit introgressions from the sister species S. paradoxus , despite the average sequence identity between these species being lower than 90%. While S. cerevisiae isolates from the Neotropics are known for their high levels of introgression, the hybridization events originating them remain unclear. Here, we sequence 216 S. cerevisiae isolates from open, spontaneous agave fermentation across Mexico. The genomes of these strains reveal considerable genetic diversity and population structure linked to geographic distribution, which had been overlooked due to undersampling of this megadiverse region. These strains, along with those from French Guiana, Ecuador, and Brazil, form a broader Neotropical phylogenetic cluster that is notably enriched in introgressions. Surprisingly, their origins and the observed conservation patterns of these introgressions indicate multiple hybridization events, suggesting flexible species barriers in this region. Our findings underscore concurrent evolutionary processes—geographical stratification and multiple introgressions—that shape the genomes of a diverse lineage of S. cerevisiae . Neotropical yeasts thus provide a natural laboratory for exploring the mechanisms and adaptive significance of introgressive hybridization in eukaryotic genome evolution. Introgression shapes eukaryotic genomes, yet its prevalence in nature remains unclear. Sequencing 216 Neotropical S. cerevisiae genomes reveals that recurrent introgression is widespread and a major driver of lineage evolution within a structured population.

Today's beer market is challenged by a decreasing consumption of traditional beer styles and an increasing consumption of specialty beers. In particular, lager-type beers (pilsner), characterized by their refreshing and unique aroma and taste, yet very uniform, struggle with their sales. The development of novel variants of the common lager yeast, the interspecific hybrid Saccharomyces pastorianus, has been proposed as a possible solution to address the need of product diversification in lager beers. Previous efforts to generate new lager yeasts through hybridization of the ancestral parental species (S. cerevisiae and S. eubayanus) yielded strains with an aromatic profile distinct from the natural biodiversity. Unfortunately, next to the desired properties, these novel yeasts also inherited unwanted characteristics. Most notably is their phenolic off-flavor (POF) production, which hampers their direct application in the industrial production processes. Here, we describe a CRISPR-based gene editing strategy that allows the systematic and meticulous introduction of a natural occurring mutation in the FDC1 gene of genetically complex industrial S. cerevisiae strains, S. eubayanus yeasts and interspecific hybrids. The resulting cisgenic POF- variants show great potential for industrial application and diversifying the current lager beer portfolio.

Several wine isolates of Saccharomyces were analysed for six molecular markers, five nuclear and one mitochondrial, and new natural interspecific hybrids were identified. The molecular characterization of these Saccharomyces hybrids was performed based on the restriction analysis of five nuclear genes (CAT8, CYR1, GSY1, MET6 and OPY1, located in different chromosomes), the ribosomal region encompassing the 5.8S rRNA gene and the two internal transcribed spacers, and sequence analysis of the mitochondrial gene COX2. This method allowed us to identify and characterize new hybrids between Saccharomyces cerevisiae and Saccharomyces kudriavzevii, between S. cerevisiae and Saccharomyces bayanus, as well as a triple hybrid S. bayanusxS. cerevisiaexS. kudriavzevii. This is the first time that S. cerevisiaexS. kudriavzevii hybrids have been described which have been involved in wine fermentation.

Abstract We examined the northern limit of Saccharomyces cerevisiae and Saccharomyces paradoxus in northeast America. We collected 876 natural samples at 29 sites and applied enrichment methods for the isolation of mesophilic yeasts. We uncovered a large diversity of yeasts, in some cases, associated with specific substrates. Sequencing of the ITS1, 5.8S and ITS2 loci allowed to assign 226 yeast strains at the species level, including 41 S. paradoxus strains. Our intensive sampling suggests that if present, S. cerevisiae is rare at these northern latitudes. Our sampling efforts spread across several months of the year revealed that successful sampling increases throughout the summer and diminishes significantly at the beginning of the fall. The data obtained on the ecological context of yeasts corroborate what was previously reported on Pichiaceae,Saccharomycodaceae,Debaryomycetaceae and Phaffomycetaceae yeast families. We identified 24 yeast isolates that could not be assigned to any known species and that may be of taxonomic, medical, or biotechnological importance. Our study reports new data on the taxonomic diversity of yeasts and new resources for studying the evolution and ecology of S. paradoxus. Natural mesophilic budding yeasts occupy specific substrates and their abundance varies during the year. Their distribution and diversity seem limited in northern latitudes of Northeast America.

Lager yeasts, Saccharomyces pastorianus, are interspecies hybrids between S. cerevisiae and S. eubayanus and are classified into Group I and Group II clades. The genome of the Group II strain, Weihenstephan 34/70, contains eight so-called ‘lager-specific’ genes that are located in subtelomeric regions. We evaluated the origins of these genes through bioinformatic and PCR analyses of Saccharomyces genomes. We determined that four are of cerevisiae origin while four originate from S. eubayanus. The Group I yeasts contain all four S. eubayanus genes but individual strains contain only a subset of the cerevisiae genes. We identified S. cerevisiae strains that contain all four cerevisiae ‘lager-specific’ genes, and distinct patterns of loss of these genes in other strains. Analysis of the subtelomeric regions uncovered patterns of loss in different S. cerevisiae strains. We identify two classes of S. cerevisiae strains: ale yeasts (Foster O) and stout yeasts with patterns of ‘lager-specific’ genes and subtelomeric regions identical to Group I and II S. pastorianus yeasts, respectively. These findings lead us to propose that Group I and II S. pastorianus strains originate from separate hybridization events involving different S. cerevisiae lineages. Using the combined bioinformatic and PCR data, we describe a potential classification map for industrial yeasts. We show that Saccharomyces pastorianus Group II yeasts are related to stout yeasts while Group I resemble ale yeasts and that the two groups arose by independent hybridization events.

Abstract Viruses are found in almost all organisms and physical habitats. One interesting example is the yeast viral ‘killer system’. The virus provides the host with a toxin directed against strains that do not carry it, while the yeast cell enables its propagation. Although yeast viruses are believed to be common, they have been actually described only for a limited number of yeast isolates. We surveyed 136 Saccharomyces cerevisiae and S. paradoxus strains of known origin and phylogenetic relatedness. Of these, 14 (c. 10%) were infected by killer viruses of one of the three types: K1, K2 or K28. As many as 34 strains (c. 25%) were not sensitive to at least one type of the killer toxin. In most cases, resistance did not disappear after attempts to cure the host strains from their viruses, suggesting that it was encoded in the host's genome. In terms of phylogeny, killer strains appear to be more related to each other than to nonkiller ones. No such tendency is observed for the phenotype of toxin resistance. Our results suggest that even if the killer toxins are not always present, they do play significant role in yeast ecology and evolution.

Saccharomyces cerevisiae and grape juice are ‘natural companions’ and make a happy wine marriage. However, this relationship can be enriched by allowing ‘wild’ non‐Saccharomyces yeast to participate in a sequential manner in the early phases of grape must fermentation. However, such a triangular relationship is complex and can only be taken to ‘the next level’ if there are no spoilage yeast present and if the ‘wine yeast’ – S. cerevisiae – is able to exert its dominance in time to successfully complete the alcoholic fermentation. Winemakers apply various ‘matchmaking’ strategies (e.g. cellar hygiene, pH, SO₂, temperature and nutrient management) to keep ‘spoilers’ (e.g. Dekkera bruxellensis) at bay, and allow ‘compatible’ wild yeast (e.g. Torulaspora delbrueckii, Pichia kluyveri, Lachancea thermotolerans and Candida/Metschnikowia pulcherrima) to harmonize with potent S. cerevisiae wine yeast and bring the best out in wine. Mismatching can lead to a ‘two is company, three is a crowd’ scenario. More than 40 of the 1500 known yeast species have been isolated from grape must. In this article, we review the specific flavour‐active characteristics of those non‐Saccharomyces species that might play a positive role in both spontaneous and inoculated wine ferments. We seek to present ‘single‐species’ and ‘multi‐species’ ferments in a new light and a new context, and we raise important questions about the direction of mixed‐fermentation research to address market trends regarding so‐called ‘natural’ wines. This review also highlights that, despite the fact that most frontier research and technological developments are often focussed primarily on S. cerevisiae, non‐Saccharomyces research can benefit from the techniques and knowledge developed by research on the former.

Brewing yeasts of the genus Saccharomyces are either available from yeast distributor centers or from breweries employing their own \"in-house strains\". During the last years, the classification and characterization of yeasts of the genus Saccharomyces was achieved by using biochemical and DNA-based methods. The current lack of fast, cost-effective and simple methods to classify brewing yeasts to a beer type, may be closed by Matrix Assisted Laser Desorption/Ionization-Time-Of-Flight Mass Spectrometry (MALDI-TOF MS) upon establishment of a database based on sub-proteome spectra from reference strains of brewing yeasts. In this study an extendable \"brewing yeast\" spectra database was established including 52 brewing yeast strains of the most important types of bottom- and top-fermenting strains as well as beer-spoiling S. cerevisiae var. diastaticus strains. 1560 single spectra, prepared with a standardized sample preparation method, were finally compared against the established database and investigated by bioinformatic analyses for similarities and distinctions. A 100% separation between bottom-, top-fermenting and S. cerevisiae var. diastaticus strains was achieved. Differentiation between Alt and Kölsch strains was not achieved because of the high similarity of their protein patterns. Whereas the Ale strains show a high degree of dissimilarity with regard to their sub-proteome. These results were supported by MDS and DAPC analysis of all recorded spectra. Within five clusters of beer types that were distinguished, and the wheat beer (WB) cluster has a clear separation from other groups. With the establishment of this MALDI-TOF MS spectra database proof of concept is provided of the discriminatory power of this technique to classify brewing yeasts into different major beer types in a rapid, easy way, and focus brewing trails accordingly. It can be extended to yeasts for specialty beer types and other applications including wine making or baking.