Molecular Mechanisms Involved in the Adaptive Evolution of Industrial Yeasts

Barrio, Eladio; González, Salvador Algarabel; Arias, Armando; Belloch, Carmela; Querol, Amparq

doi:10.1007/978-3-540-28398-0_6

Cited by 30 publications

(28 citation statements)

References 79 publications

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“…Various mechanisms are known to be involved in the adaptive evolution of yeasts to the fermentation process, such as gene duplication, polyploidy, chromosomal rearrangements, interspecific hybridization, and introgression (28). Recent analyses have shown that yeast hybrids may be more abundant in both natural and industrial environments than previously thought.…”

Section: Discussionmentioning

confidence: 99%

Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118

Novo

Bigey

Beyne

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

392

484

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Saccharomyces cerevisiae has been used for millennia in winemaking, but little is known about the selective forces acting on the wine yeast genome. We sequenced the complete genome of the diploid commercial wine yeast EC1118, resulting in an assembly of 31 scaffolds covering 97% of the S288c reference genome. The wine yeast differed strikingly from the other S. cerevisiae isolates in possessing 3 unique large regions, 2 of which were subtelomeric, the other being inserted within an EC1118 chromosome. These regions encompass 34 genes involved in key wine fermentation functions. Phylogeny and synteny analyses showed that 1 of these regions originated from a species closely related to the Saccharomyces genus, whereas the 2 other regions were of non-Saccharomyces origin. We identified Zygosaccharomyces bailii, a major contaminant of wine fermentations, as the donor species for 1 of these 2 regions. Although natural hybridization between Saccharomyces strains has been described, this report provides evidence that gene transfer may occur between Saccharomyces and nonSaccharomyces species. We show that the regions identified are frequent and differentially distributed among S. cerevisiae clades, being found almost exclusively in wine strains, suggesting acquisition through recent transfer events. Overall, these data show that the wine yeast genome is subject to constant remodeling through the contribution of exogenous genes. Our results suggest that these processes are favored by ecologic proximity and are involved in the molecular adaptation of wine yeasts to conditions of high sugar, low nitrogen, and high ethanol concentrations. adaptive evolution ͉ comparative genomics ͉ horizontal gene transfer ͉ introgression ͉ Zygosaccharomyces bailii

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Section: Discussionmentioning

confidence: 99%

Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118

Novo

Bigey

Beyne

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

392

484

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“…The hybridization in Saccharomyces sensu stricto complex is often thought to be one of the evolutionary models for wine yeasts, according to which the conjugating spores and haploid cells of different, usually homothallic strains, give rise to new strains (Lopes et al. 2002; Barrio et al. 2006; Sipiczki 2008; Querol and Bond 2009).…”

Section: Introductionmentioning

confidence: 99%

Physiological and genetic stability of hybrids of industrial wine yeasts Saccharomyces sensu stricto complex

Kunicka-Styczyńska

Rajkowska

2011

Journal of Applied Microbiology

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Aims: The aim of this study was to examine the physiological and genetic stability of hybrids of industrial wine yeasts Saccharomyces sensu stricto complex subjected to acidic stress during fermentation. Methods and Results: Laboratory‐constructed yeast hybrids, one intraspecific Saccharomyces cerevisiae × S. cerevisiae and three interspecific S. cerevisiae ×Saccharomyces bayanus, were subcultured in aerobic or anaerobic conditions in media with or without l‐malic acid. Changes in the biochemical profiles, karyotypes and mitochondrial DNA profiles of the segregates were assessed after 50–190 generations. All yeast segregates showed a tendency to increase the range of the tested compounds utilized as sole carbon sources. Interspecific hybrids were alloaneuploid and their genomes tended to undergo extensive rearrangement especially during fermentation. The karyotypes of segregates lost up to four and appearance up to five bands were recorded. The changes in their mtDNA patterns were even broader reaching 12 missing and six additional bands. These hybrids acquired the ability to sporulate and significantly changed their biochemical profiles. The alloaneuploid intraspecific S. cerevisiae hybrid was characterized by high genetic stability despite the phenotypic changes. l‐malic acid was not found to affect the extent of genomic changes of the hybrids, which suggests that their demalication ability is combined with resistance to acidic stress. Conclusions: The results reveal the plasticity and extent of changes of chromosomal and mitochondrial DNA of interspecific hybrids of industrial wine yeast especially under anaerobiosis. They imply that karyotyping and restriction analysis of mitochondrial DNA make it possible to quickly assess the genetic stability of genetically modified industrial wine yeasts but may not be applied as the only method for their identification and discrimination. Significance and Impact of the Study: Laboratory‐constructed interspecific hybrids of industrial strains may provide a model for studying the adaptive evolution of wine yeasts under fermentative stress.

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“…Additional genomic variation can arise from interspecific hybridization, which can occur between two or more Saccharomyces species (for reviews, see Barrio et al 2006;Sipiczki 2008;Querol and Bond 2009;Dujon 2010), e.g., S. cerevisiae-S. kudriavzevii hybrid wine and brewing yeasts (e.g., Bradbury et al 2006;Gonzalez et al 2008), S. cerevisiae-S. uvarum hybrid cider and brewing yeasts (e.g., Masneuf et al 1998;de Barros Lopes et al 2002;Rainieri et al 2006), and the most well-known hybrid, the lager yeast S. pastorianus, which is an interspecific hybrid between S. cerevisiae and the recently described S. eubayanus (Libkind et al 2011). Furthermore, introgression events, defined as a relatively small region of a different species' genome found within the genome of another species and mostly occurring within the closely related species of the Saccharomyces sensu stricto group, have also been detected (Naumova et al 2005;Liti et al 2006;Doniger et al 2008;Muller and McCusker 2009a,b;Naumova et al 2011).…”

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confidence: 99%

Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments

Dunn¹,

Richter²,

Kvitek³

et al. 2012

Genome Res.

201

182

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Although the budding yeast Saccharomyces cerevisiae is arguably one of the most well-studied organisms on earth, the genome-wide variation within this species—i.e., its “pan-genome”—has been less explored. We created a multispecies microarray platform containing probes covering the genomes of several Saccharomyces species: S. cerevisiae, including regions not found in the standard laboratory S288c strain, as well as the mitochondrial and 2-μm circle genomes–plus S. paradoxus, S. mikatae, S. kudriavzevii, S. uvarum, S. kluyveri, and S. castellii. We performed array-Comparative Genomic Hybridization (aCGH) on 83 different S. cerevisiae strains collected across a wide range of habitats; of these, 69 were commercial wine strains, while the remaining 14 were from a diverse set of other industrial and natural environments. We observed interspecific hybridization events, introgression events, and pervasive copy number variation (CNV) in all but a few of the strains. These CNVs were distributed throughout the strains such that they did not produce any clear phylogeny, suggesting extensive mating in both industrial and wild strains. To validate our results and to determine whether apparently similar introgressions and CNVs were identical by descent or recurrent, we also performed whole-genome sequencing on nine of these strains. These data may help pinpoint genomic regions involved in adaptation to different industrial milieus, as well as shed light on the course of domestication of S. cerevisiae.

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Molecular Mechanisms Involved in the Adaptive Evolution of Industrial Yeasts

Cited by 30 publications

References 79 publications

Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118

Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118

Physiological and genetic stability of hybrids of industrial wine yeasts Saccharomyces sensu stricto complex

Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments

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