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The genetic basis of organisms’ adaptation to different environments is a central issue of molecular evolution. The budding yeast Saccharomyces cerevisiae and its relatives predominantly ferment glucose into ethanol even in the presence of oxygen. This was suggested to be an adaptation to glucose-rich habitats, but the underlying genetic basis of the evolution of aerobic fermentation remains unclear. In S. cerevisiae, the first step of glucose metabolism is transporting glucose across the plasma membrane, which is carried out by hexose transporter proteins. Although several studies have recognized that the rate of glucose uptake can affect how glucose is metabolized, the role of HXT genes in the evolution of aerobic fermentation has not been fully explored. In this study, we identified all members of the HXT gene family in 23 fully sequenced fungal genomes, reconstructed their evolutionary history to pinpoint gene gain and loss events, and evaluated their adaptive significance in the evolution of aerobic fermentation. We found that the HXT genes have been extensively amplified in the two fungal lineages that have independently evolved aerobic fermentation. In contrast, reduction of the number of HXT genes has occurred in aerobic respiratory species. Our study reveals a strong positive correlation between the copy number of HXT genes and the strength of aerobic fermentation, suggesting that HXT gene expansion has facilitated the evolution of aerobic fermentation.

Large-scale population genomic surveys are essential to explore the phenotypic diversity of natural populations. Here we report the whole-genome sequencing and phenotyping of 1,011 Saccharomyces cerevisiae isolates, which together provide an accurate evolutionary picture of the genomic variants that shape the species-wide phenotypic landscape of this yeast. Genomic analyses support a single ‘out-of-China’ origin for this species, followed by several independent domestication events. Although domesticated isolates exhibit high variation in ploidy, aneuploidy and genome content, genome evolution in wild isolates is mainly driven by the accumulation of single nucleotide polymorphisms. A common feature is the extensive loss of heterozygosity, which represents an essential source of inter-individual variation in this mainly asexual species. Most of the single nucleotide polymorphisms, including experimentally identified functional polymorphisms, are present at very low frequencies. The largest numbers of variants identified by genome-wide association are copy-number changes, which have a greater phenotypic effect than do single nucleotide polymorphisms. This resource will guide future population genomics and genotype–phenotype studies in this classic model system. Whole-genome sequencing of 1,011 natural isolates of the yeast Saccharomyces cerevisiae reveals its evolutionary history, including a single out-of-China origin and multiple domestication events, and provides a framework for genotype–phenotype studies in this model organism.

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.

NRC publication: Yes

The yeast Saccharomyces cerevisiae has been an essential component of human civilization because of its long global history of use in food and beverage fermentation. However, the diversity and evolutionary history of the domesticated populations of the yeast remain elusive. We show here that China/Far East Asia is likely the center of origin of the domesticated populations of the species. The domesticated populations form two major groups associated with solid- and liquid-state fermentation and appear to have originated from heterozygous ancestors, which were likely formed by outcrossing between diverse wild isolates primitively for adaptation to maltose-rich niches. We found consistent gene expansion and contraction in the whole domesticated population, as well as lineage-specific genome variations leading to adaptation to different environments. We show a nearly panoramic view of the diversity and life history of S. cerevisiae and provide new insights into the origin and evolution of the species. An understanding of the domestication of the yeast Saccharomyces cerevisiae has important implications for studying its evolution and diversity. Here, the authors show that Far East Asia is likely the center of origin of the domesticated populations of the yeast based on genomic and phenotypic characterization of a large collection of isolates.

The self-templating conformations of yeast prion proteins act as epigenetic elements of inheritance. Yeast prions might provide a mechanism for generating heritable phenotypic diversity that promotes survival in fluctuating environments and the evolution of new traits. However, this hypothesis is highly controversial. Prions that create new traits have not been found in wild strains, leading to the perception that they are rare ‘diseases’ of laboratory cultivation. Here we biochemically test approximately 700 wild strains of Saccharomyces for [ PSI + ] or [ MOT3 + ], and find these prions in many. They conferred diverse phenotypes that were frequently beneficial under selective conditions. Simple meiotic re-assortment of the variation harboured within a strain readily fixed one such trait, making it robust and prion-independent. Finally, we genetically screened for unknown prion elements. Fully one-third of wild strains harboured them. These, too, created diverse, often beneficial phenotypes. Thus, prions broadly govern heritable traits in nature, in a manner that could profoundly expand adaptive opportunities. Previously thought to be rare laboratory artefacts or diseases of yeast, prions are actually found in one third of 700 wild strains; the prions give their hosts beneficial traits that can be transmitted epigenetically to the next generation, and then fixed in the genome. Natural prions give yeasts the edge It has been suggested that prions — proteins that undergo transmissible conformation changes — serve as elements of inheritance and evolutionary 'facilitators' in yeast, but many still consider fungal prions to be rare laboratory 'diseases'. Now Susan Lindquist and colleagues have screened 700 yeast strains collected from the wild and found 'natural' prions in one-third of them. They also show that many of these natural prions endow their hosts with traits that are either directly beneficial in specific culture conditions or provide favourable ground for further, DNA-based traits to evolve.

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.

Domestication of plants and animals promoted humanity's transition from nomadic to sedentary lifestyles, demographic expansion, and the emergence of civilizations. In contrast to the well-documented successes of crop and livestock breeding, processes of microbe domestication remain obscure, despite the importance of microbes to the production of food, beverages, and biofuels. Lager-beer, first brewed in the 15th century, employs an allotetraploid hybrid yeast, Saccharomyces pastorianus (syn. Saccharomyces carlsbergensis ), a domesticated species created by the fusion of a Saccharomyces cerevisiae ale-yeast with an unknown cryotolerant Saccharomyces species. We report the isolation of that species and designate it Saccharomyces eubayanus sp. nov. because of its resemblance to Saccharomyces bayanus (a complex hybrid of S. eubayanus , Saccharomyces uvarum , and S. cerevisiae found only in the brewing environment). Individuals from populations of S. eubayanus and its sister species, S. uvarum , exist in apparent sympatry in Nothofagus (Southern beech) forests in Patagonia, but are isolated genetically through intrinsic postzygotic barriers, and ecologically through host-preference. The draft genome sequence of S. eubayanus is 99.5% identical to the non- S. cerevisiae portion of the S. pastorianus genome sequence and suggests specific changes in sugar and sulfite metabolism that were crucial for domestication in the lager-brewing environment. This study shows that combining microbial ecology with comparative genomics facilitates the discovery and preservation of wild genetic stocks of domesticated microbes to trace their history, identify genetic changes, and suggest paths to further industrial improvement.

Abstract Kombucha, historically an Asian tea-based fermented drink, has recently become trendy in Western countries. Producers claim it bears health-enhancing properties that may come from the tea or metabolites produced by its microbiome. Despite its long history of production, microbial richness and dynamics have not been fully unraveled, especially at an industrial scale. Moreover, the impact of tea type (green or black) on microbial ecology was not studied. Here, we compared microbial communities from industrial-scale black and green tea fermentations, still traditionally carried out by a microbial biofilm, using culture-dependent and metabarcoding approaches. Dominant bacterial species belonged to Acetobacteraceae and to a lesser extent Lactobacteriaceae, while the main identified yeasts corresponded to Dekkera, Hanseniaspora and Zygosaccharomyces during all fermentations. Species richness decreased over the 8-day fermentation. Among acetic acid bacteria, Gluconacetobacter europaeus, Gluconobacter oxydans, G. saccharivorans and Acetobacter peroxydans emerged as dominant species. The main lactic acid bacteria, Oenococcus oeni, was strongly associated with green tea fermentations. Tea type did not influence yeast community, with Dekkera bruxellensis, D. anomala, Zygosaccharomyces bailii and Hanseniaspora valbyensis as most dominant. This study unraveled a distinctive core microbial community which is essential for fermentation control and could lead to Kombucha quality standardization. Microbial ecology of industrial Kombucha fermentations.

Many crops display differential geographic phenotypes and sensorial signatures, encapsulated by the concept of terroir . The drivers behind these differences remain elusive and the potential contribution of microbes has been ignored until recently. Significant genetic differentiation between microbial communities and populations from different geographic locations has been demonstrated, but crucially it has not been shown whether this correlates with differential agricultural phenotypes or not. Using wine as a model system, we utilize the regionally genetically differentiated population of Saccharomyces cerevisiae in New Zealand and objectively demonstrate that these populations differentially affect wine phenotype, which is driven by a complex mix of chemicals. These findings reveal the importance of microbial populations for the regional identity of wine and potentially extend to other important agricultural commodities. Moreover, this suggests that long-term implementation of methods maintaining differential biodiversity may have tangible economic imperatives as well as being desirable in terms of employing agricultural practices that increase responsible environmental stewardship.