Chapter 6: The genomes of lager yeasts.
TL;DR: In response to exposure to environmental stresses such as high temperatures and high osmotic pressure, the genomes appear to be highly dynamic and undergo recombination events at defined loci and alterations in the telomeric regions.
Abstract: Yeasts used in the production of lagers belong to the genus Saccharomyces pastorianus. Species within this genus arose from a natural hybridization event between two yeast species that appear to be closely related to Saccharomyces cerevisiae and Saccharomyces bayanus. The resultant hybrids contain complex allopolyploid genomes and retain genetic characteristics of both parental species. Recent genome analysis using both whole genome sequencing and competitive genomic hybridization techniques has revealed the underlying composition of lager yeasts genomes. There appear to be at least 36 unique chromosomes, many of which are lager specific, resulting from recombination events between the homeologous parental chromosomes. The recombination events are limited to a defined set of genetic loci, which are highly conserved within strains of lager yeasts. In addition to the hybrid chromosomes, several non-reciprocal chromosomal translocations and inversions are also observed. Remarkably, in response to exposure to environmental stresses such as high temperatures and high osmotic pressure, the genomes appear to be highly dynamic and undergo recombination events at defined loci and alterations in the telomeric regions. The ability of environmental stress to alter the structure and composition of the genomes of lager yeasts may point to mechanisms of adaptive evolution in these species.
Citations
More filters
TL;DR: 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: 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.
560 citations
TL;DR: It is found that the S. eubayanus subgenomes of lager-brewing yeasts have experienced increased rates of evolution since hybridization, and that certain genes involved in metabolism may have been particularly affected.
Abstract: The dramatic phenotypic changes that occur in organisms during domestication leave indelible imprints on their genomes. Although many domesticated plants and animals have been systematically compared with their wild genetic stocks, the molecular and genomic processes underlying fungal domestication have received less attention. Here, we present a nearly complete genome assembly for the recently described yeast species Saccharomyces eubayanus and compare it to the genomes of multiple domesticated alloploid hybrids of S. eubayanus × S. cerevisiae (S. pastorianus syn. S. carlsbergensis), which are used to brew lager-style beers. We find that the S. eubayanus subgenomes of lager-brewing yeasts have experienced increased rates of evolution since hybridization, and that certain genes involved in metabolism may have been particularly affected. Interestingly, the S. eubayanus subgenome underwent an especially strong shift in selection regimes, consistent with more extensive domestication of the S. cerevisiae parent prior to hybridization. In contrast to recent proposals that lager-brewing yeasts were domesticated following a single hybridization event, the radically different neutral site divergences between the subgenomes of the two major lager yeast lineages strongly favor at least two independent origins for the S. cerevisiae × S. eubayanus hybrids that brew lager beers. Our findings demonstrate how this industrially important hybrid has been domesticated along similar evolutionary trajectories on multiple occasions.
175 citations
Cites background from "Chapter 6: The genomes of lager yea..."
...…microbes achieve tremendous population sizes, lineages can adaptively lose the ability to reproduce sexually when passaged vegetatively (Lang et al. 2009), while other lineages are derived from sterile interspecies hybrids (Querol and Bond 2009; Borneman et al. 2012; Gibson and Liti 2015)....
[...]
...Because ale strains are the most likely S. cerevisiae parent of lager-brewing yeasts (Dunn and Sherlock 2008; Querol and Bond 2009; Monerawela et al. 2015), MAL genes were also extracted from the publicly available genomes of the ale strains Foster’s O and Foster’s B (Borneman et al. 2011)....
[...]
...…of Lager-Brewing Yeasts The single origin (Walther et al. 2014; Wendland 2014) and multiple origin (Liti et al. 2005; Dunn and Sherlock 2008; Bond 2009) hypotheses for the origins of lager yeasts make distinct predictions about the divergences that would be expected between the S. eubayanus…...
[...]
...One hypothesis proposes that the Saaz and Frohberg lineages resulted from independent hybridization events (Liti et al. 2005; Dunn and Sherlock 2008; Bond 2009)....
[...]
TL;DR: In this article, the authors sequenced S. carlsbergensis using next generation sequencing technologies and showed that the 19.5-Mb genome is substantially larger than the S. cerevisiae genome.
Abstract: Lager yeast beer production was revolutionized by the introduction of pure culture strains. The first established lager yeast strain is known as the bottom fermenting Saccharomyces carlsbergensis, which was originally termed Unterhefe No. 1 by Emil Chr. Hansen and has been used in production in since 1883. S. carlsbergensis belongs to group I/Saaz-type lager yeast strains and is better adapted to cold growth conditions than group II/Frohberg-type lager yeasts, e.g., the Weihenstephan strain WS34/70. Here, we sequenced S. carlsbergensis using next generation sequencing technologies. Lager yeasts are descendants from hybrids formed between a S. cerevisiae parent and a parent similar to S. eubayanus. Accordingly, the S. carlsbergensis 19.5-Mb genome is substantially larger than the 12-Mb S. cerevisiae genome. Based on the sequence scaffolds, synteny to the S. cerevisae genome, and by using directed polymerase chain reaction for gap closure, we generated a chromosomal map of S. carlsbergensis consisting of 29 unique chromosomes. We present evidence for genome and chromosome evolution within S. carlsbergensis via chromosome loss and loss of heterozygosity specifically of parts derived from the S. cerevisiae parent. Based on our sequence data and via fluorescence-activated cell-sorting analysis, we determined the ploidy of S. carlsbergensis. This inferred that this strain is basically triploid with a diploid S. eubayanus and haploid S. cerevisiae genome content. In contrast the Weihenstephan strain, which we resequenced, is essentially tetraploid composed of two diploid S. cerevisiae and S. eubayanus genomes. Based on conserved translocations between the parental genomes in S. carlsbergensis and the Weihenstephan strain we propose a joint evolutionary ancestry for lager yeast strains.
120 citations
01 Jan 2014
TL;DR: Evidence for genome and chromosome evolution within S. carlsbergensis via chromosome loss and loss of heterozygosity specifically of parts derived from the S. cerevisiae parent is presented and a joint evolutionary ancestry for lager yeast strains is proposed.
111 citations
Cites background from "Chapter 6: The genomes of lager yea..."
...…parent is viewed to be a close relative of S. eubayanus, and the S. cerevisiae Volume 4 May 2014 | S. carlsbergensis Genome | 791 parent may have been a strain already used for beer brewing, e.g., an ale yeast (Dunn and Sherlock 2008; Bond 2009; Libkind et al. 2011; Nguyen et al. 2011)....
[...]
...Lager yeasts are interspecies hybrids between S. cerevisiae and S. uvarum parents (Nilsson-Tillgren et al. 1986; Kielland-Brandt et al. 1995; Casaregola et al. 2001; Bond 2009)....
[...]
TL;DR: This article shows that an osmotolerant yeast species, Pichia sorbitophila, recently isolated in a concentrated sorbitol solution in industry, illustrates this last situation and finds that the physiological characteristics of this new yeast species are determined by specific but unequal contributions of its two parents.
Abstract: Polyploidization is an important process in the evolution of eukaryotic genomes, but ensuing molecular mechanisms remain to be clarified. Autopolyploidization or whole-genome duplication events frequently are resolved in resulting lineages by the loss of single genes from most duplicated pairs, causing transient gene dosage imbalance and accelerating speciation through meiotic infertility. Allopolyploidization or formation of interspecies hybrids raises the problem of genetic incompatibility (Bateson-Dobzhansky-Muller effect) and may be resolved by the accumulation of mutational changes in resulting lineages. In this article, we show that an osmotolerant yeast species, Pichia sorbitophila, recently isolated in a concentrated sorbitol solution in industry, illustrates this last situation. Its genome is a mosaic of homologous and homeologous chromosomes, or parts thereof, that corresponds to a recently formed hybrid in the process of evolution. The respective parental contributions to this genome were characterized using existing variations in GC content. The genomic changes that occurred during the short period since hybrid formation were identified (e.g., loss of heterozygosity, unilateral loss of rDNA, reciprocal exchange) and distinguished from those undergone by the two parental genomes after separation from their common ancestor (i.e., NUMT (NUclear sequences of MiTochondrial origin) insertions, gene acquisitions, gene location movements, reciprocal translocation). We found that the physiological characteristics of this new yeast species are determined by specific but unequal contributions of its two parents, one of which could be identified as very closely related to an extant Pichia farinosa strain.
106 citations
Cites background or result from "Chapter 6: The genomes of lager yea..."
...If stress conditions in cultures have been invoked to stimulate the formation of yeast hybrids (Belloch et al. 2008; Querol and Bond 2009), experiments show that yeast species in general tend to have no or limited prezygotic barriers (Chou et al. 2010; Greig et al. 2002; Liti et al. 2006; Marinoni…...
[...]
...On one hand, we observed a diploid level for this genome, in contrast to aneuploid situations reported for hybrids of the genus Saccharomyces (Querol and Bond 2009), probably attributable to the hybridization event that generated directly a strict allodiploid hybrid (Gerstein et al. 2006)....
[...]
...Querol, A., and U. Bond, 2009 The complex and dynamic genomes of industrial yeasts....
[...]
...Several interspecific hybrids have been described among species that belong to the genus Saccharomyces and play key roles in industrial fermentations (Bond et al. 2009; Dunn and Sherlock 2008; Nakao et al. 2009; Querol and Bond 2009; Rainieri et al. 2006; Sipiczki 2008)....
[...]
References
More filters
TL;DR: A growing amount of evidence indicates that polyploid cells also arise during a variety of pathological conditions, and genetic instability in these cells might provide a route to aneuploidy and thereby contribute to the development of cancer.
Abstract: Polyploidy is a frequent phenomenon in the eukaryotic world, but the biological properties of polyploid cells are not well understood. During evolution, polyploidy is thought to be an important mechanism that contributes to speciation. Polyploid, usually non-dividing, cells are formed during development in otherwise diploid organisms. A growing amount of evidence indicates that polyploid cells also arise during a variety of pathological conditions. Genetic instability in these cells might provide a route to aneuploidy and thereby contribute to the development of cancer.
789 citations
"Chapter 6: The genomes of lager yea..." refers background in this paper
..., 1992) and are known to have higher rates of genome instability compared to haploid strains (Mayer and Aguilera, 1990; Storchova and Pellman, 2004)....
[...]
TL;DR: The causes and consequences of instability are reviewed with the aim of providing a mechanistic perspective on the origin of genomic instability.
Abstract: Genomic instability in the form of mutations and chromosome rearrangements is usually associated with pathological disorders, and yet it is also crucial for evolution. Two types of elements have a key role in instability leading to rearrangements: those that act in trans to prevent instability--among them are replication, repair and S-phase checkpoint factors--and those that act in cis--chromosomal hotspots of instability such as fragile sites and highly transcribed DNA sequences. Taking these elements as a guide, we review the causes and consequences of instability with the aim of providing a mechanistic perspective on the origin of genomic instability.
753 citations
TL;DR: The results suggest intimate association between man and wine yeast across centuries, and hypothesize that yeast followed man and vine migrations as a commensal member of grapevine flora.
Abstract: Fermented beverages and foods have played a significant role in most societies worldwide for millennia. To better understand how the yeast species Saccharomyces cerevisiae , the main fermenting agent, evolved along this historical and expansion process, we analysed the genetic diversity among 651 strains from 56 different geographical origins, worldwide. Their genotyping at 12 microsatellite loci revealed 575 distinct genotypes organized in subgroups of yeast types, i.e. bread, beer, wine, sake. Some of these groups presented unexpected relatedness: Bread strains displayed a combination of alleles intermediate between beer and wine strains, and strains used for rice wine and sake were most closely related to beer and bread strains. However, up to 28% of genetic diversity between these technological groups was associated with geographical differences which suggests local domestications. Focusing on wine yeasts, a group of Lebanese strains were basal in an F ST tree, suggesting a Mesopotamia-based origin of most wine strains. In Europe, migration of wine strains occurred through the Danube Valley, and around the Mediterranean Sea. An approximate Bayesian computation approach suggested a postglacial divergence (most probable period 10 000–12 000 BP ). As our results suggest intimate association between man and wine yeast across centuries, we hypothesize that yeast followed man and vine migrations as a commensal member of grapevine flora.
511 citations
Additional excerpts
...bayanus (de Barros Lopes et al., 2002; Legras et al., 2007)....
[...]
TL;DR: This review describes the mechanisms and consequences of replication stalling at various natural impediments, with an emphasis on the role of replicationStalling in genomic instability.
Abstract: Summary: Accurate and complete replication of the genome in every cell division is a prerequisite of genomic stability. Thus, both prokaryotic and eukaryotic replication forks are extremely precise and robust molecular machines that have evolved to be up to the task. However, it has recently become clear that the replication fork is more of a hurdler than a runner: it must overcome various obstacles present on its way. Such obstacles can be called natural impediments to DNA replication, as opposed to external and genetic factors. Natural impediments to DNA replication are particular DNA binding proteins, unusual secondary structures in DNA, and transcription complexes that occasionally (in eukaryotes) or constantly (in prokaryotes) operate on replicating templates. This review describes the mechanisms and consequences of replication stalling at various natural impediments, with an emphasis on the role of replication stalling in genomic instability.
492 citations
"Chapter 6: The genomes of lager yea..." refers background in this paper
...There is a growing body of evidence suggesting that natural impediments to replication fork progression can lead to gross chromosomal rearrangements (Azvolinsky et al., 2006; Huang and Koshland, 2003; Lemoine et al., 2005; Mirkin and Mirkin, 2007; Schmidt and Kolodner, 2006)....
[...]
TL;DR: This paper reviewed aspects of stress and stress response in the context of baker's yeast manufacturing and applications, and discussed the potential for improving the general robustness of industrial baker yeast strains, in relation to physiological and genetic manipulations.
Abstract: Application of yeasts in traditional biotechnologies such as baking, brewing, distiller's fermentations, and wine making, involves them in exposure to numerous environmental stresses. These can be encountered in concert and sequentially. Yeast exhibit a complex array of stress responses when under conditions that are less than physiologically ideal. These responses involve aspects of cell sensing, signal transduction, transcriptional and posttranslational control, protein-targeting to organelles, accumulation of protectants, and activity of repair functions. The efficiency of these processes in a given yeast strain determines its robustness, and to a large extent, whether it is able to perform to necessary commercial standards in industrial processes. This article reviews aspects of stress and stress response in the context of baker's yeast manufacturing and applications, and discusses the potential for improving the general robustness of industrial baker's yeast strains, in relation to physiological and genetic manipulations.
442 citations
"Chapter 6: The genomes of lager yea..." refers background in this paper
...Lager yeasts are exposed to high osmotic and hydrostatic pressure, anaerobiosis, low pH, low temperature, high alcohol concentrations and high cell densities during fermentation (Attfield, 1997; Brosnan et al., 2000; Carrasco et al., 2001; Gibson et al., 2008; Zuzuarregui et al., 2005)....
[...]