The Yeast Genomics* lab @ NOVA

(*evolutionary, functional, comparative and more)

The beginning of agriculture and the domestication of plants and animals are among the most decisive events in the past 13,000 years of human history. Archaeological and biomolecular evidence indicates that rice wine was produced as far back as 7,000 BC in China. In Zagros mountains in Iran, wine was produced 5,000 BC and the domestication of barley in the Fertile Crescent led to the emergence of the forebear of modern beer in Sumeria 4,000 BC. Furthermore, yeast cells were detected in Egyptian leavened bread dough dated 3,000 BC and molecular evidence for the presence of Saccharomyces cerevisiae in wine fermentation has been obtained from pottery jars of the same period.

Ethanol and many other metabolites contributed to preserve dietary goods and opened the way for the production of a myriad of alcoholic beverages that become important in social habits of many civilizations.
In spite of their long association to the fermentation of foods and beverages, the natural biology of Saccharomyces remains elusive. Little is known about the ecology of the seven natural species and their biology outside the laboratory still has many mysteries.

Through extensive field studies in temperate oak forests in different continents and equivalent biotopes in the Southern Hemisphere we aim at a better understanding of the natural history of Saccharomyces. We are specifically interested in discovering wild populations and to perform whole-genome comparisons with domesticated lineages. We reason that such endeavors will provide a new ecological framework for the understanding of the diverse cellular, molecular, and evolutionary mechanisms that shaped the world’s most biotechnologically important microbe. Here are some recent highlights of our work:

Yeast Evolutionary Ecology and Domestication

José Paulo Sampaio

We reported in PNAS the identification in Patagonia of Saccharomyces eubayanus, one of the ancestors of the complex hybrid genome of lager yeast (Saccharomyces pastorianus). This study involved the isolation of dozens of strains of S. eubayanus and its sister species S. uvarum from Nothofagus (Southern beech) and Cyttaria, its biotrophic fungal parasite. We detected S. eubayanus and S. uvarum in sympatry, but found that the two species were genetically isolated through a post-zygotic barrier and 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. The discovery of S. eubayanus and of the origins of S. pastorianus solved a controversy of decades.

(read the full story here)

(portuguese press coverage of this research here)

Detection of Saccharomyces eubayanus in Patagonia

S. eubayanus sp. nov. is distinct from S. uvarum and donated its genome to S. pastorianus.

A model of the formation of S. pastorianus and the hybrid strains of S. bayanus

We reported in Nature Communications a population genomics study of the cider and wine yeast S. uvarum using the most comprehensive strain dataset currently available and involving new isolates collected by us in New Zealand, Tasmania, and in South and North America. We revealed a highly diverse South American population containing more genetic diversity than that found in the Northern Hemisphere. Moreover we documented that a Patagonian sub-population gave rise to the Holarctic population through a recent bottleneck. We were surprised to find that the European isolates displayed multiple introgressions from other Saccharomyces species, those from S. eubayanus being prevalent in European strains associated with human-driven fermentations. These introgressions were normally absent in wild strains and gene ontology analyses indicated that several gene categories relevant for wine fermentation were overrepresented. Such findings constitute a first indication of domestication in S. uvarum.

(read the full story here)

(portuguese press coverage of this research here)

The global phylogeography and the first indication of domestication in Saccharomyces uvarum

Geographic distribution, phylogeny and population structure of S. uvarum

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

The Mediterranean origins of wine yeast domestication

The domestication of the wine yeast Saccharomyces cerevisiae is thought to be contemporary with the development of viticulture along the Mediterranean basin. Until recently, the unavailability of wild lineages prevented the identification of the closest wild relatives of wine yeasts. To bridge this gap, we used whole-genome data of a balanced number of anthropic and natural S. cerevisiae strains. We identified industrial variants and new geographically delimited populations, including a novel Mediterranean oak population that turned out to be the closest relative of the wine lineage. A model considering partial isolation with asymmetrical migration (mostly wild group >> wine group), was found to be best supported by the data and, notably, the divergence time estimates between the two populations agree with historical evidence for winemaking. Besides, three horizontally transmitted regions previously described to contain genes relevant to wine fermentation, are present in the Wine group but not in the Mediterranean oak group. This represents a major discontinuity between the two populations and is likely to denote a domestication fingerprint in wine yeasts. Taken together, these results indicate that Mediterranean oaks harbour the wild genetic stock of domesticated wine yeasts. This work was published in Molecular Ecology and a commentary on the paper appears in the News and Views section of the journal.

(read the full story here)

(read the accompanied commentary here)

(portuguese press coverage of this research here)

Population structure and admixture in Saccharomyces cerevisiae

The global diversity of Saccharomyces cerevisiae is shaped by both ecology and geography. Neighbour-net network of 146 strains based on 60 331 SNPs.

Whole-genome phylogenetic relationships between 112 “clean” non-mosaic Saccharomyces cerevisiae strains inferred from 193 071 SNPs.

Natural hybridization in Brazilian wild lineages of S. cerevisiae

The global distribution of natural populations of S. cerevisiae, especially in tropical regions such as Brazil were oaks and other members of the Fagaceae are absent, is not well understood. In the work recently published in Genome Biology and Evolution we investigated the occurrence of S. cerevisiae in Brazil, and reported a candidate natural habitat of S. cerevisiae in South America. Using whole-genome data, we uncovered new lineages that appear to have as closest relatives the wild populations found in North America and Japan. Population structure analysis revealed the penetration of the wine genotype into the wild Brazilian population, providing the first clear observation of the impact of domesticated microbe lineages on the genetic structure of wild populations. Widespread introgression from the American S. paradoxus population into the newly uncovered Brazilian population was also evident.

We hypothesize that hybridization in tropical wild lineages may have facilitated the habitat transition accompanying the colonization of the tropical ecosystem.

(read the full story here)

Population structure of S. cerevisiae. Migrant strains are marked with colored diamonds: red (isolated in Brazil), green (isolated in Europe), and blue (isolated in North America). Yellow circles depict non-Brazilian strains with partial Brazilian ancestry.

Saccharomyces cerevisiae X S. paradoxus hybrid genomes

Whole-genome phylogeny of 143 strains of S. cerevisiae inferred from 69,321 SNPs. Representatives of the new wild lineages from Brazil indicated as B1, B2, B3, and B4