The metabolic domestication syndrome of budding yeast
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Roland Tengölics Balázs Szappanos Michael Mülleder Dorottya Kalapis Gábor Grézal Csilla Sajben Federica Agostini João Benhur Mokochinski Balázs Bálint László G Nagy Markus Ralser Balázs PappAbstract
Cellular metabolism evolves through changes in the structure and quantitative states of metabolic networks. Here, we explore the evolutionary dynamics of metabolic states by focusing on the collection of metabolite levels, the metabolome, which captures key aspects of cellular physiology. Using a phylogenetic framework, we profiled metabolites in 27 populations of nine budding yeast species, providing a graduated view of metabolic variation across multiple evolutionary time scales. Metabolite levels evolve more rapidly and independently of changes in the metabolic network’s structure, providing complementary information to enzyme repertoire. Although metabolome variation accumulates mainly gradually over time, it is profoundly affected by domestication. We found pervasive signatures of convergent evolution in the metabolomes of independently domesticated clades of Saccharomyces cerevisiae. Such recurring metabolite differences between wild and domesticated populations affect a substantial part of the metabolome, including rewiring of the TCA cycle and several amino acids that influence aroma production, likely reflecting adaptation to human niches. Overall, our work reveals previously unrecognized diversity in central metabolism and the pervasive influence of human-driven selection on metabolite levels in yeasts.
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Volume
121
Issue number
11
Pages
e2313354121
Available online
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10.1073/pnas.2313354121
Europe PubMed Central
38457520
Pubmed
38457520
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