Revealing the natural history of yeast

The following is a guest post by Matthew Vandermeulen, PhD, at the University at Buffalo. Matthew studies the regulation of responses to environmental variation; he is on Twitter as @mvandermeulen.

Saccharomyces cerevisiae, baker’s and brewer’s yeastmay be one organism that could contend with dogs for the title of man’s best friend.  Saccharomyces cerevisiae has been associated with human culture for thousands of years for use in baking and making alcoholic beverages. In modern times, yeast has become a model to study cell and molecular biology: it was the first eukaryote to have a fully sequenced genome, and it has been reprogrammed to produce pharmaceuticals.  The economic and cultural value of S. cerevisiae has led to debates on what type of evolutionary processes have shaped this organism’s natural history — but to this day we don’t know where, exactly, yeast was first “domesticated” for human uses. 

It was once believed that S. cerevisiae evolved exclusively in man-made environments with no wild habitat after an ancient ancestor adapted to the domesticated lifestyle and diverged. Then, S. cerevisiae began to be isolated from wild settings, like oak forests, and clinical settings as pathogens, so scientists began speculating about its natural origin. Some have hypothesized that the origin of domestication of S. cerevisiae may have originated in AfricaMesopotamia, or Europe. However, in 2012 this view point began to shift when a group of scientists isolated and sequenced yeast strains from primeval (undisturbed by humans) forests in China and hypothesized that the origin of domesticated S. cerevisiae lineages was in China/Far East Asia. 

Figure 1 from Duan et al. (2018). The phylogeny (a) and population structure (b) of wild and domesticated S. cerevisiae from China. Primeval forest strains (green) are significantly diverged from domesticated strains (red/blue/purple).

Since then, numerous studies have further supported this claim, such as a study from the same lab in 2018, which isolated and sequenced even more wild and domesticated strains from China, a study using a large sequenced global collection of yeast, a study isolating and analyzing wild strains from Taiwan, and a study incorporating long read sequencing dataAdditionally, extensive surveys from other regions have failed to find similar primeval yeast strains, including EuropeNorth AmericaSouth AmericaAfrica, and New Zealand, although the lack of finding primeval strains in these regions cannot conclusively say they are not present.

In the study by Duan et al., in 2018, they found that domesticated Chinese yeast strains from Asia have more genetic diversity than domesticated lineages from any other continent. The domesticated Chinese lineages also show that they underwent a genetic bottleneck from the primeval forest strains found in China (Figure 1). This genetic diversity and bottleneck have been seen by other studies as well. Duan et alfound the bottleneck breaks into two major domesticated lineages, solid state and liquid state fermentative strains, suggesting that strains from both fermentative states have a common ancestor.  The solid-state fermentation process, where fermentation occurs on a solid substrate, is native to Far East Asia along with the strains involved in those processes.  This suggests that the liquid state fermentation strains (like those involved in making beer and wine) most likely originate from Far East Asia as well because of their common ancestry.  Further evidence comes by the finding that domesticated strains share a common expansion and contraction of certain genes regardless of the fermented sources they were isolated from. For example, extra copies of genes associated with Maltose utilization are found in all domesticated lineages, even in lineages that are not associated with maltose utilization, such as liquid state fermentation strains. This suggests both solid state and liquid state lineages have a common ancestor that originated in China/Far East Asia.

The China/Far East Asia hypothesis has been challenged by a previous study that suggested wine strains were first domesticated in Europe.  Duan et al. showed, through three major finds, that the wine strains in Europe were actually transferred from Asia. First, the global wine lineage (which includes the European strains) has four strains that originate from Asia. Second, the European strains share horizontal gene transfers with the Chinese wine strains and the primeval strains. It is unlikely that the Chinese wine strains obtained the horizontal gene transfers from European strains and then transferred them to the primeval strains, especially when the domesticated Chinese strains show signatures of a genetic bottleneck from the primeval forest populations. Third, the wine and milk lineages share a common ancestor and the milk lineage ancestor is from China, making the wine strain ancestry also from China. So, it seems unlikely that S. cerevisiae originated in Europe and is more likely to have originated in China/Far East Asia.

Finding China/Far East Asia to be the origin of domestication and natural habitat of S. cerevisiae has perks. For one, it informs scientists where to study the wildest ancestral strains to further our understanding of S. cerevisiae natural history. Perhaps a resolution can even be made for the long-standing debate about whether S. cerevisiae evolution has been mainly driven by natural selection or neutral genetic drift. Duan et al. and other studies support genetic drift as the major evolutionary process in wild S. cerevisiae diversification. One of the reasons is because a correlation has not been established between geographic/ecological factors and the genetic diversity in wild strains. However, this reasoning cannot be considered conclusive because much of S. cerevisiae ecology is still unknown and the correct ecological factors may have yet to be explored. Another reason genetic drift is supported as the major evolutionary force is because strong signs of purifying or positive selection have not been found in the regions tested of the wild strains’ genomes. Again, this reasoning is also not conclusive because not finding signs of selection does not completely rule out its occurrence, and future studies may be able to identify parts of the genome under selection.  

Finding the wild strains and habitats of S. cerevisiae can also help inform scientists about the organism’s ecology. For example, Duan et al. looked for selection differences between wild and domesticated lineages and found the domesticated lineages appear to have been under clear artificial selection based on human-altered-ecological niches. One of the effects of domestication is that the FLO-gene family (a family of major cell adhesion molecules in yeast) experiences contraction or loss in domesticated lineages. This raises the ecological question of why adhesion properties are maintained in wild strains, but not domesticated strains, and suggests cell adhesion is important for yeast ecology. Wild strains have also informed scientists about S. cerevisiae immigration and reproduction in natural settings because different wild lineages are found sympatric (i.e. in the same habitat) suggesting that immigration seems to be common in nature, yet wild populations appear to remain reproductively isolated according to very low admixture (Figure 1). What mechanism leads to reproductive isolation of wild S. cerevisiae? Some studies have suggested chromosomal rearrangements, while Duan et al. suggest possibly large introgressed regions of horizontal gene transfer or lineage specific copy number variations are the cause.  Future work will be needed to disentangle this complex question.

So, overall, isolating and sequencing wild strains from China/Far East Asia has led to new understandings over the last decade about the ecology and natural history of this highly influential organism. These strains have driven many scientists to agree that the natural habitat and origin of domestication of S. cerevisiae is forests in China/Far East Asia. However, one cannot help but wonder, if more and more extensive surveys continue to be conducted on other continents, could more primeval strains be uncovered and change our viewpoint once again?


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About Jeremy Yoder

Jeremy B. Yoder is an Assistant Professor of Biology at California State University Northridge, studying the evolution and coevolution of interacting species, especially mutualists. He is a collaborator with the Joshua Tree Genome Project and the Queer in STEM study of LGBTQ experiences in scientific careers. He has written for the website of Scientific American, the LA Review of Books, the Chronicle of Higher Education, The Awl, and Slate.
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