Evidence for two main domestication trajectories inSaccharomyces cerevisiaelinked to distinct bread-making processes

Abstract

Keywords yeast, tetraploid, Saccharomyces, sourdough, bread 1 2 3 4 5 6 7 8 9 10 11 12 13 14 SummaryDespite bread being one of the most historically and culturally important fermented products, its history and influence on the evolution of associated microbial species remains largely unknown. The first evidence of leavened bread dates to the second millenium BCE in Egypt and since, the art of bread-making developed and spread worldwide. Nowadays, leavened bread is made either by using a pure commercial culture of the yeast Saccharomyces cerevisiae or by propagating a sourdough, which is a mix of flour and water spontaneously fermented by yeast and bacteria. We studied the domestication of S. cerevisiae populations originating from industry and sourdough and tested whether these different bread-making processes led to population divergence. We found that the origin of S. cerevisiae bakery strains is polyphyletic with 67 % of strains clustering in two main clades: most commercial strains were tetraploid and clustered with strains having diverse origins, including beer. By contrast, most sourdough strains were diploids and found in a second clade of strains having mosaic genomes and diverse origins including fruits, or clinical and wild environments. When compared to the others, sourdough strains harboured in average a higher copy number of genes involved in maltose utilization, a common sugar produced from dough starch. Overall, a high level of gene flow from multiple contributors was detected. Phenotyping of bakery and non bakery strains further showed that sourdough and industrial bakery populations have undergone human selection for rapidly starting fermentations and for high CO 2 production. Interestingly, sourdough strains also showed a better adaptation to a sourdough mimicking environment, suggesting that natural selection occurred as well. In summary, our results revealed that the domestication of bakery yeast populations has been accompanied by dispersion, hybridization and divergent selection through industrial and artisanal bakery processes. In addition, they unveiled for the first time a case of fungus domestication where species divergence occurred through autotetraploidisation.

History and Domestication of Saccharomyces cerevisiae in Bread Baking

“…The ability to ferment maltose is variable across species and strains of yeast (Bell et al, 2001;Houghton-Larsen and Brandt, 2006;Naumova et al, 2013), with commercial baking Baking strains tend to have multiple copies of MAL loci and/or MAL genes. Duval et al, 2010;Bigey et al, 2020 Glucose suppression…”

“…Until quite recently, large-scale genomic studies of baking strains have been non-existent, and more work is still needed to tie together the history of bread with the genetic history of these strains. This gap in knowledge is beginning to be rectified, with new phylogenetic analyses of commercial and sourdough baking strains illuminating a polyphyletic origin of baking strains ( Peter et al, 2018 ; Bigey et al, 2020 ). Bakery strains surveyed thus far are largely from European isolates, and fall into two major clades, suggesting at least two domestication events leading to commercial baking strains and sourdough baking strains, respectively ( Bigey et al, 2020 ).…”

“…This gap in knowledge is beginning to be rectified, with new phylogenetic analyses of commercial and sourdough baking strains illuminating a polyphyletic origin of baking strains ( Peter et al, 2018 ; Bigey et al, 2020 ). Bakery strains surveyed thus far are largely from European isolates, and fall into two major clades, suggesting at least two domestication events leading to commercial baking strains and sourdough baking strains, respectively ( Bigey et al, 2020 ). Within these two clades, both noted for their mixed origins, the bakery strains are interspersed with strains isolated from many sources including wine, sake, clinical, and natural environments.…”

“…Despite the intertwined history of beer and breadmaking, the phylogenetic relationships of beer and bread strains are largely separated. There are a few exceptions, including African maize dough strains clustering with African beer strains, and a subset of beer strains clustering with mixed origin bakery strains ( Bigey et al, 2020 ). Surprisingly, no sequenced bakery strains cluster with Ale beer strains, although there is evidence of Ale beer strain introgression in some of the bakery strains ( Bigey et al, 2020 ).…”

“…Baking strains tend to have more complex genetic architecture compared to laboratory strains ( Steensels et al, 2014a ), and fewer genes are differentially expressed in baking strains compared to domesticated wine and beer strains during dough fermentation ( Aslankoohi et al, 2013 ). Commercial baking strains tend to be a higher ploidy (up to 68% of baking strains have a ploidy above 2n) and have higher rates of aneuploidy (up to 17% of baking strains are aneuploid) than wild and semi-wild sourdough strains (up to 35% are polyploid or aneuploid) ( Bigey et al, 2020 ). Tetraploidization appears to have occurred at least once in the domestication of commercial baking strains, and translates to a significantly faster start of fermentation compared to diploid strains ( Bigey et al, 2020 ).…”