Biogeography, population genetics and rapid centromere evolution in Saccharomyces cerevisiae
Lead Research Organisation:
University of Manchester
Department Name: Life Sciences
Abstract
Saccharomyces cerevisiae is the species of yeast that puts the alcohol into sake, wine and beer and is used to make bread. Some S. cerevisiae strains also live independently of humans in the bark of oak trees and the soil around them. Partly because sake, wine, beer and bread are so interesting and partly because this single-celled fungus is so simple yet has much in common with animal and plant cells, researchers have studied it in the laboratory for decades. Now S. cerevisiae is probably better understood at the cellular and molecular level than any animal, plant or other fungus, yet little is known about its ecology. This study will lead to a better understanding of S. cerevisiae in Europe and how far they migrate and mix with their relatives in different habitats and geographic locations. S. cerevisiae has been discovered in the bark of oak trees in North America, South East Asia and various other parts of the world, they have also been found in soils from Holland and Finland, but they have not yet been discovered in the oaks of Europe. In a recent study, scientists in North America discovered that pretreating bark and soil with alcohol and sugar led to the isolation of S. cerevisiae, even though their occurrence in bark and soil would otherwise rarely be noticed. The use of this technique is likely to lead to the discovery of S. cerevisiae in European oaks. In this study, small amounts of soil, bark or grapes will be taken back to the lab and analysed for the presence of yeasts. The DNA sequences of the yeasts that are discovered in this way are studied for signs of genetic subdivision. If there are signs that different types of DNA sequence prevail among the yeasts from different habitats or different geographic regions, then that suggests that there has been little or no admixture between these sites now or even in the last few thousand years. The level of difference among the DNA sequences from different sites can lead to an estimate of approximately how long it has been since there was reasonable mixture between the yeasts of different habitats or regions. This study will use what is probably the most rapidly evolving type of DNA sequence in yeasts - the centromere - something that changes fast is most likely to pick up the differences among even very similar yeasts, and so will minimise the amount of DNA sequence necessary to spot differences. Though useful for the purposes of this study, the rapid evolution of centromeres is also very curious. Centromeres play a crucial role in any kind of cell division. They form the points at which the cell's machinery attaches to all the genetic material of a cell and organises the equal division of DNA into the next generation of cells. Laboratory experiments in the 1980s showed that certain types of change to the DNA sequence of a centromere resulted in various types of failure, from the most devastating failures in growth and reproduction to reduced fertility among a yeast's offspring. Why would something so important be evolving so fast? Might this rapid evolution have consequences for growth, fertility or the reproductive isolation between species? I will also use the data from the investigation into yeast ecology to address this question. These data from natural populations together with a couple of simple laboratory experiments should reveal the causes and consequences of rapid centromere evolution.
People |
ORCID iD |
Douda Bensasson (Principal Investigator) |
Publications
Tsai IJ
(2008)
Population genomics of the wild yeast Saccharomyces paradoxus: Quantifying the life cycle.
in Proceedings of the National Academy of Sciences of the United States of America
Tilakaratna V
(2016)
Habitat predicts levels of genetic admixture in Saccharomyces cerevisiae
Tilakaratna V
(2017)
Habitat Predicts Levels of Genetic Admixture in Saccharomyces cerevisiae.
in G3 (Bethesda, Md.)
Robinson HA
(2016)
Summer temperature can predict the distribution of wild yeast populations.
in Ecology and evolution
Nielsen KM
(2007)
Release and persistence of extracellular DNA in the environment.
in Environmental biosafety research
Martin FN
(2007)
Mitochondrial genome sequences and comparative genomics of Phytophthora ramorum and P. sojae.
in Current genetics
Liti G
(2009)
Population genomics of domestic and wild yeasts.
in Nature
Keller I
(2007)
Transition-Transversion Bias Is Not Universal: A Counter Example from Grasshopper Pseudogenes
in PLoS Genetics
Carr M
(2012)
Evolutionary genomics of transposable elements in Saccharomyces cerevisiae.
in PloS one
Description | Most people do not realise that Saccharomyces cerevisiae, the species of yeast used to make wine, beer and bread, also lives wild in the bark of oak trees. Indeed evidence from this project suggests that old growth forest is probably the ancestral habitat of wine yeast. Our analysis of DNA sequence of a worldwide sample of wine yeast shows that the wine yeasts used from Europe to Chile, North America and Australia, trace their origins to somewhere near Europe and are much more closely related to yeast from oak trees in Europe than those from North America. S. cerevisiae living in oak trees show the patterns of isolation by distance typically seen in plants and animals. S. cerevisiae isolated from oak trees in North Carolina are distinct from those in Pennsylvania, and distinct populations reside in the oaks of Portugal, Hungary and Greece. This and our other population genetic analyses show that contrary to many people's expectations, yeasts in woodland habitats live in small isolated populations, where they are unaffected by domestication. We also find evidence that S. cerevisiae is rare or nonexistent in the bark of oaks in the UK, and we propose that UK summers are to cold for wild wine yeast. Few microbial species ranges have ever been described before, and it is a worrying thought that microbes as well as plants and animals might be sensitive to climate change. |
Exploitation Route | At the end of this project we also generated genome sequence for over 70 yeast genomes. These genomes are already used as a resource by my team and other scientists, to answer questions about basic science and genetic biodiversity. We are currently submitting the data to the public databases for genome sequence. In addition, we recently predicted the wild species distribution for the wine yeast Saccharomyces cerevisiae. This prediction should be very useful for other scientists wishing to use this model organism to better understand the behaviour of microbes in the natural environment. |
Sectors | Agriculture, Food and Drink,Environment |
URL | http://planetearth.nerc.ac.uk/features/story.aspx?id=579 |
Description | I am not aware of how our findings have been used outside of academia so far. |
Title | A collection of wild yeast strains |
Description | A collection of wild yeast strains from woodlands and fruit in the UK (Peak District, New Forest, Surrey and East Anglia), from the South of France, and from various locations in Greece. I plan to send these strains to the UK National Centre for Yeast Cultures in East Anglia, for curation and distribution to labs across the world. |
Type Of Material | Biological samples |
Year Produced | 2011 |
Provided To Others? | Yes |
Impact | We used the collection of these strains to document the predict the worldwide species distributions of Saccharomyces cerevisiae and Saccharomyces paradoxus. The manuscript for this work is almost complete: Robinson, H.A., Pinharanda A., Bensasson, D. (in prep) "Some like it hot: the distribution of Saccharomyces yeast in Europe". A PhD student I co-supervise is also using some of these strains to study the biogeography of S. paradoxus within Europe. Daniela Delneri is using a Saccharomyces kudriavzevii to study adaptation to temperature. I plan to use these strains to study patterns of yeast genetic diversity within Europe. |
Title | Genome data for over 70 strains of Saccharomyces cerevisiae |
Description | Next Generation Sequencing (Illumina) of over 70 strains of Saccharomyces cerevisiae publicly available at the European Nucleotide Archive (PRJEB7601). Most of these strains are from 3 distinct wild populations from 2 woodlands in Japan and 1 woodland in Portugal. These data will allow us to estimate many population genetic parameters for wild yeast populations. |
Type Of Material | Database/Collection of data |
Year Produced | 2012 |
Provided To Others? | Yes |
Impact | Members of the Bergman lab at Manchester and others have used these data since 2012, and the data were released publicly at EBI in 2015. Our recent paper on these data has already attracted several citations: Almeida, Pedro, Raquel Barbosa, Polona Zalar, Yumi Imanishi, Kiminori Shimizu, Benedetta Turchetti, Jean-Luc Legras, et al. 'A Population Genomics Insight into the Mediterranean Origins of Wine Yeast Domestication'. Molecular Ecology 24, no. 21 (1 November 2015): 5412-27. doi:10.1111/mec.13341. and a News and Views article in Molecular Ecology: Eberlein, Chris, Jean-Baptiste Leducq, and Christian R. Landry. 'The Genomics of Wild Yeast Populations Sheds Light on the Domestication of Man's Best (micro) Friend'. Molecular Ecology 24, no. 21 (1 November 2015): 5309-11. doi:10.1111/mec.13380. |
URL | http://www.ebi.ac.uk/ena/data/view/PRJEB7601 |
Description | Collaboration with Jose Sampaio in the Universidade Nova de Lisboa, Portugal |
Organisation | New University of Lisbon |
Country | Portugal |
Sector | Academic/University |
PI Contribution | I contributed genome sequences, yeast strains, expertise, training and supervision in evolutionary biology, bioinformatics and genome analysis. |
Collaborator Contribution | Many more yeast strains than I could have collected in Northern Europe, an FCT funded PhD student, Pedro Almeida, who I co-supervise. |
Impact | The following manuscript is ready for submission: Almeida, P., Barbosa, R. Zalar, P., Legras, J-L., Dequin, S., Turchetti, B., Bensasson, D., Gonc¸alvez, P., Sampaio, J.P. (in prep) "Mediterranean oaks harbor the wild genetic stock of domesticated wine yeasts". Genome sequences are being submitted to the EBI - SRA for genome sequences, under the following project number: PRJEB7601 |
Start Year | 2009 |
Description | Article for NERC's Planet Earth magazine |
Form Of Engagement Activity | A magazine, newsletter or online publication |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Public/other audiences |
Results and Impact | This magazine reaches a broad range of people. I am not aware of the impact of the article (except that it reached a lot of academics who mentioned it) as well as members of the public |
Year(s) Of Engagement Activity | 2009 |
URL | http://www.nerc.ac.uk/publications/planetearth/2009/winter/win09-yeast.pdf |
Description | Royal Society - MP pairing scheme |
Form Of Engagement Activity | Participation in an open day or visit at my research institution |
Part Of Official Scheme? | Yes |
Geographic Reach | National |
Primary Audience | Policymakers/politicians |
Results and Impact | My MP started to visit our University open days, and we have corresponded a few times since this activity. I was interviewed by a journalist from the Guardian about my participation: http://www.guardian.co.uk/science/2012/may/18/scientists-duty-pipette-placard |
Year(s) Of Engagement Activity | 2011,2012 |
URL | https://royalsociety.org/training/pairing-scheme/ |
Description | school visit (Manchester) |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Schools |
Results and Impact | The kids (aged 5-6) loved learning about the life of a scientist, conducting experiments (highly related to my fellowship), and learning about the invisible world of microbes. Contrary to many of the stereotypes children receive at this age, I think it is also important that kids see that women can be successful scientists. Most of the children asked brilliant questions that showed I had held their attention and they ended up with an excellent understanding of yeast and microbial ecology. I have been asked to return every year (and I will because I enjoyed this activity), parents reported learning a lot from their children and I have heard that one young girl who planned to be singers is now considering a career in science. |
Year(s) Of Engagement Activity | 2013 |