A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum

Abstract

In addition to Saccharomyces cerevisiae, the cryotolerant yeast species S. uvarum is also used for wine and cider fermentation but nothing is known about its natural history. Here we use a population genomics approach to investigate its global phylogeography and domestication fingerprints using a collection of isolates obtained from fermented beverages and from natural environments on five continents. South American isolates contain more genetic diversity than that found in the Northern Hemisphere. Moreover, coalescence analyses suggest that a Patagonian sub-population gave rise to the Holarctic population through a recent bottleneck. Holarctic strains display multiple introgressions from other Saccharomyces species, those from S. eubayanus being prevalent in European strains associated with human-driven fermentations. These introgressions are absent in the large majority of wild strains and gene ontology analyses indicate that several gene categories relevant for wine fermentation are overrepresented. Such findings constitute a first indication of domestication in S. uvarum.

Fig. 1. Geographic distribution, phylogeny, and population structure of Saccharomyces uvarum

A, Maximum Likelihood (ML) phylogeny of the genus Saccharomyces based on a concatenated alignment of 14 gene sequences and rooted with Naumovozyma castellii. Representatives of populations of S. paradoxus (EUR, European; FE, Far Eastern; and NA, North American) and of the Australasian (AUST) and Holarctic (HOL) populations of S. uvarum are included. Support values correspond to 100 bootstrap replicates and branch lengths correspond to the mean number of nucleotide substitutions per site. B, World map depicting the geographic origin of Holarctic and Australasian S. uvarum strains. C, Map of South America depicting the collecting sites. Locations are indicated by capital letters surrounded by light- or dark-orange colored circles corresponding to populations SA-A and SA-B, respectively. The co-occurrence of strains of the two populations is depicted by light-and dark-orange semi-circles, and the occurrence of mosaic strains is depicted by white contour lines. The distribution of Nothofagus is shown in green. D, Whole-genome Neighbor-Joining (NJ) phylogeny of 54 strains based on 129096 SNPs and excluding introgressed regions from S. eubayanus, inferred with p-distance and rooted with S. eubayanus. The three main clades are marked by letters A, B, and C. Support values from 1000 bootstrap NJ and ML (RAxML rapid bootstrap) trees are included. Incongruent topologies between NJ and ML are denoted by grey lines. Branch lengths correspond to the mean number of base differences per site. Strains isolated from natural environments are marked by blue circles whereas strains isolated from anthropic environments are marked by red circles. Strains having introgressions are marked with an “I” in a yellow (introgressions from S. eubayanus), blue (introgressions from S. kudriavzevii), or orange (introgressions from S. cerevisiae) diamond. For the hybrid strains (marked with an “H” in a white circle) or S. bayanus (“B” in a white circle), only introgressions in the S. uvarum sub-genome are depicted. South American mosaic strains are marked with an “M” in an orange square. Clusters inferred with STRUCTURE considering all sequences (A) and all but the Australasian sequences (B) are depicted.

Fig. 2. Proportion of shared and privately segregating polymorphisms and coalescence analysis in the South American and Holarctic populations

A, Proportion of private alleles, fixed differences, and shared polymorphisms among SNPs found in all possible pairwise comparisons involving the Holarctic (HOL) and the two South American populations, SA-A and SA-B (South American mosaic strains were excluded from the analysis). B, Genome-wide estimation of relative time to coalescence for the Holarctic and the two South American populations. The tree was built from an alignment of 51159 high quality sites (Phred quality score >Q40) partitioned over the 16 chromosomes. Each partition represents regions without evidence for intra-locus recombination. The scale bar depicts estimated substitutions per site. Node ages are printed in bold near the nodes of the population whose coalescence they estimate. Branch lengths are printed in italics above the branches. One representative strain of the divergent Australasian population was used to root the tree. The insert shows the marginal posterior densities of the time to the most recent common ancestor (tmrca) in each population.

Fig. 3. Sliding window analysis of Saccharomyces eubayanus introgressions in S. uvarum genomes

Each plot represents the divergence k (with Jukes-Cantor correction) relative to S. eubayanus reference strain CRUB 1568. Introgressed strains are color-coded according to the key.

Fig. 4. Chromosome maps of S. uvarum strains showing the location and extent of introgressions from S. eubayanus

The maps are shown for the 16 strains that have S. eubayanus introgressions (hybrid strains excluded).