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Colonies of Saccharomyces cerevisiae bread yeast growing on a nutrient agar medium. © INRA, CAIN Anne-Hélène

The remarkable genomic evolution of cheese and wine yeasts

Bread, wine, cheese, rum or oak bark…. How has the Saccharomyces cerevisiae yeast shaped its genome to adapt to these different environments? An international team led by scientists from INRA, working in collaboration with CEA, has compared the genomes of 82 strains of this yeast. They have revealed strikingly specific features concerning the strains isolated in wine and cheese. Published in Molecular Biology and Evolution on 8 May 2018, their studies show that the genome of this yeast has been shaped by the environmental constraints of man-made media.

Updated on 06/01/2018
Published on 05/07/2018

Saccharomyces cerevisiae is the principal yeast involved in the leavening of bread and the fermentation of wine or rum. It is also found in cheese and the bark of oak trees. But although the phylogeny of this species is well known, we still do not understand how this yeast is able to adapt to these different environments.
  
Scientists from INRA, working in collaboration with CEA and teams from Portugal and Spain, have compared the genomes of 82 strains of the S. cerevisiae yeast. They identified groups of strains from wine, flor wine [1], rum, bread, cheese (and fermented milk) and oak trees. They showed that each of these groups displayed specific genomic traits; for example, the presence or absence of certain genes, variations in the number of gene copies or mutations modifying their protein properties. These data thus provided clues to their ecological specialisation. Most of the strains – when compared with the genome of the reference strain – possessed additional genetic elements resulting from similar (introgression) or distant (horizontal transfer) species, several of which were common to strains arising from the same ecological niche.

 The contrasted evolution of wine and cheese yeasts

Although they probably have a common genetic origin, wine and cheese strains display very particular specialisations. In cheese, yeasts are highly effective in metabolising galactose (a sugar arising from the hydrolysis of milk lactose by other micro-organisms during cheese development) but they are inefficient regarding the fermentation of sugars present in grape must (such as glucose and fructose). By contrast, wine strains are better able to ferment grape juice and grow more slowly on galactose than cheese strains.
  
This greater capacity of cheese strains to utilise galactose could be explained by the presence of a group of genes (GAL7-GAL10-GAL1) implicated in galactose metabolism. Although this group is present in other strains of the S. cerevisiae species, in cheese yeasts it corresponds to a more efficient ancestral version which arose from a species that does not belong to the currently recognised group of Saccharomyces. In addition, cheese yeasts present a highly differentiated galactose transporter. When combined, these two genomic traits may facilitate the development of these strains in cheese. On the other hand, the genome of cheese strains has lost various genes coding for glucose transporters, thus explaining their poor performance in the context of wine fermentation.
 
Furthermore, the scientists demonstrated that wine yeasts also display signs of specific adaptation. These strains contain variations in the genes implicated in using amino acids and phytosterols (nutrients in grapes that are essential to yeast growth).
 
This study has confirmed the results obtained previously by the same team [2]: through horizontal transfer, these yeasts have acquired genes that enable them to use the sources of nitrogen in grapes more efficiently. By domesticating yeasts for wine fermentation, humans have empirically selected genomic variations and gene exchanges between genetically distant species. Similarly, S. cerevisiae has shaped its genome in order to adapt to the environment of cheese or fermented milk.

This phylogenetic tree represents the family relationships between different S. cerevisiae strains/individuals.  The colours indicate groups of strains that resemble each other. These groups also correspond to different habitats: the yeasts have adapted to a particular habitat/process.. © INRA
This phylogenetic tree represents the family relationships between different S. cerevisiae strains/individuals.  The colours indicate groups of strains that resemble each other. These groups also correspond to different habitats: the yeasts have adapted to a particular habitat/process. © INRA

[1] Vins de voile (wines raised under flor yeast) are produced using a specific process that exploits the oenological virtues of a natural veil of yeast (S. cerevisiae) that gradually develops on the surface of cask-aged wines that are not “ouillé” (i.e. the cask is not regularly topped up to prevent oxidation of the wine during ageing). This veil protects the wine from bacteria and oxidation throughout the process. Vins de voile include sherry and "yellow wine" from the Jura region.

[2] Novo M, Bigey F, Beyne E, Galeote V, Gavory F, Mallet S, Cambon B, Legras JL, Wincker P, Casaregola S, Dequin S.Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118.PNAS U S A. 2009 Sep 22;106 (38):16333-8.doi: 10.1073/pnas.0904673106.

Marsit, S., Mena, A., Bigey, F., Sauvage, F. X., Couloux, A., Guy, J., Legras, J. L., Barrio, E., Dequin, S., Galeote, V. (2015).Evolutionary advantage conferred by an eukaryote-to-eukaryote gene transfer event in wine yeasts.Molecular Biology and Evolution, 32 (7), 1695-1707

Coi AL, Bigey F, Mallet S, Marsit S, Zara G, Gladieux P, Galeote V, Budroni M, Dequin S, Legras J-L. 2017. Genomic signatures of adaptation to wine biological ageing conditions in biofilm-forming flor yeasts. Mol. Ecol.38:42–49

http://doi.wiley.com/10.1111/ijlh.12426

Contact(s)
Scientific contact(s):

  • Jean-Luc Legras (33 (0)4 99 61 31 70) Sciences for Oenology Joint Research Unit (Université de Montpellier 1, INRA, Montpellier SupAgro)
Press Relations:
INRA News Office (33 (0)1 42 75 91 86)
Associated Division(s):
Microbiology and the Food Chain
Associated Centre(s):
Occitanie-Montpellier

Reference

Jean-Luc Legras, Virginie Galeote, Frédéric Bigey, Carole Camarasa, Souhir Marsit, Thibault Nidelet, Isabelle Sanchez, Arnaud Couloux, Julie Guy, Ricardo Franco-Duarte, Marina Marcet-Houben, Toni Gabaldon, Dorit Schuller, José Paulo Sampaio, Sylvie Dequin Adaptation of S. cerevisiae to fermented food environments reveals remarkable genome plasticity and the footprints of domestication. Molecular Biology and Evolution 2018, doi:10.1093/molbev/msy066