Genomic instability in an interspecific hybrid of the genus Saccharomyces: a matter of adaptability

Abstract

Ancient events of polyploidy have been linked to huge evolutionary leaps in the tree of life, while increasing evidence shows that newly established polyploids have adaptive advantages in certain stress conditions compared to their relatives with a lower ploidy. The genus Saccharomyces is a good model for studying such events, as it contains an ancient whole-genome duplication event and many sequenced Saccharomyces cerevisiae are, evolutionary speaking, newly formed polyploids. Many polyploids have unstable genomes and go through large genome erosions; however, it is still unknown what mechanisms govern this reduction. Here, we sequenced and studied the natural S. cerevisiae × Saccharomyces kudriavzevii hybrid strain, VIN7, which was selected for its commercial use in the wine industry. The most singular observation is that its nuclear genome is highly unstable and drastic genomic alterations were observed in only a few generations, leading to a widening of its phenotypic landscape. To better understand what leads to the loss of certain chromosomes in the VIN7 cell population, we looked for genetic features of the genes, such as physical interactions, complex formation, epistatic interactions and stress responding genes, which could have beneficial or detrimental effects on the cell if their dosage is altered by a chromosomal copy number variation. The three chromosomes lost in our VIN7 population showed different patterns, indicating that multiple factors could explain the mechanisms behind the chromosomal loss. However, one common feature for two out of the three chromosomes is that they are among the smallest ones. We hypothesize that small chromosomes alter their copy numbers more frequently as a low number of genes is affected, meaning that it is a by-product of genome instability, which might be the chief driving force of the adaptability and genome architecture of this hybrid.

The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae

“…Saccharomyces cerevisiae is one of the descendants of this ancestral hybridization event, currently maintaining a third of its genome in duplicate [5,6,10]. In more recent works, it has been demonstrated that hybridization events among wine yeasts are produced mainly through rare mating types, giving rise to new hybrids with differential duplicated chromosome retention linked to adaptive functional innovation [11][12][13]. These works support the prevalence of duplicates and innovative potential as proposed more than fifty years ago by Ohno [14].…”

How to characterize a strain? Clonal heterogeneity in industrial Saccharomyces influences both phenotypes and heterogeneity in phenotypes

“…However, studies comparing Saccharomyces strains rarely address the “founder effect” of using a subclone lineage of a strain (due to methodological constraints) to characterize the strain itself. Only a few studies have focused on heterogeneous subclone lineages as well as cryptic variation of the PE‐2 bioethanol strain or its derivative JAY270 (Reis et al, 2014; Rodrigues‐Prause et al, 2018; Sampaio et al, 2019) and those of the lager W34/70 strain (Bolat et al, 2008; van den Broek et al, 2015), as well as on lineages on the VIN7 commercial hybrid wine starter yeast (Morard et al, 2020), whereas in most other cases, strains are used interchangeably with subclone lineages in literature. In fact, the commonly used and well‐known tetraploid Ale strain has been sequenced and analyzed by three recent studies.…”

“…A number of clades have become adapted to the production of fermented beverages or foods, and these are regarded as prime examples of microbe domestication that quite often led to the existence of polyploid and/or aneuploid lineages (Duan et al, 2018; Gallone et al, 2016; Peter et al, 2018; Steensels et al, 2019; Strope et al, 2015). The most widespread yeast‐fermented product worldwide that uses a different yeast “species” is lager beer, where fermentation is carried out by domesticated hybrids of S. cerevisiae and Saccharomyces eubayanus (known as Saccharomyces pastorianus and Saccharomyces carlsbergensis as well), whereas hybrids of other combinations have also been found in several fermentation industries (Gallone et al, 2019; Langdon et al, 2019; Morard et al, 2020; Salazar et al, 2019).…”

“…The latter include ploidy changes, aneuploidies/chromosome copy number variations (CCNVs), loss of heterozygosity (LOH), gross chromosomal rearrangements (GCRs), and mitotic crossing overs (Peter et al, 2018; van den Broek et al, 2015; Zhu et al, 2016). These phenomena can alter their industrial performance and may happen very rapidly (Gorter de Vries et al, 2020; Kadowaki et al, 2017; Large et al, 2020; Morard et al, 2019, 2020; Zhang et al, 2016). Along with point mutations, these GSV events result in clonal populations gradually accumulating differences in various traits, leading to clonal heterogeneity, clonal interference (competition among isogenic asexual lineages), and hence the emergence of so‐called subclonal lineages, reminiscent of the experimental evolution setups conducted with laboratory strains (Blundell et al, 2018; Lang et al, 2011; Large et al, 2020; Payen et al, 2016).…”

Evidence of Biparental Mitochondrial Inheritance from Self-Fertile Crosses between Closely Related Species of Ceratocystis

“…Here, we used a novel approach to demonstrate that self-fertile isolates of different Ceratocystis species can hybridize and that their progeny often bears the mitochondria of both parental species. Although the importance of hybridization during adaptation and evolution is widely recognized [ 45 , 46 ], fungal hybridization is not completely understood, and few studies have explored the level to which sexual reproductive barriers and species boundaries are permeable [ 47 , 48 ]. By employing cultures grown from single ascospore drops obtained from crosses between C. fimbriata and C. manginecans and between C. fimbriata and C. eucalypticola, we showed, for the first time, that self-fertile isolates of closely related Ceratocystis species can sexually reproduce, forming viable progeny with mitochondrial inheritance from both parents.…”