Abstract
Yeasts are known to have versatile metabolic traits, while how these metabolic traits have evolved has not been elucidated systematically. We performed integrative evolution analysis to investigate how genomic evolution determines trait generation by reconstructing genome‐scale metabolic models (GEMs) for 332 yeasts. These GEMs could comprehensively characterize trait diversity and predict enzyme functionality, thereby signifying that sequence‐level evolution has shaped reaction networks towards new metabolic functions. Strikingly, using GEMs, we can mechanistically map different evolutionary events, e.g. horizontal gene transfer and gene duplication, onto relevant subpathways to explain metabolic plasticity. This demonstrates that gene family expansion and enzyme promiscuity are prominent mechanisms for metabolic trait gains, while GEM simulations reveal that additional factors, such as gene loss from distant pathways, contribute to trait losses. Furthermore, our analysis could pinpoint to specific genes and pathways that have been under positive selection and relevant for the formulation of complex metabolic traits, i.e. thermotolerance and the Crabtree effect. Our findings illustrate how multidimensional evolution in both metabolic network structure and individual enzymes drives phenotypic variations.
Highlights
Budding yeasts are unicellular fungi with > 1,000 known species
We annotated all of the studied genomes in detail (Appendix Fig S1A-1I), yielding the ideal input for reconstruction of a yeast pan-genome-scale metabolic models (GEMs) and species-specific GEMs (ssGEMs) (Fig 1A, Appendix Fig S1J), as well as systematic analyses of fungal genome evolution, such as horizontal gene transfer events, gene family expansion and gene evolution rate estimation (Fig 1B)
The pan-genome-scale metabolic model (pan-GEM) comprises of metabolic reactions and enzymes from all 343 fungal species, containing a total of 3,135 metabolites, 4,599 reactions and 3,751 ortholog groups, which represents a significant expansion of coverage in metabolism compared with a prior fungal pan-GEM (Correia & Mahadevan, 2020) (Appendix Fig S1J)
Summary
Budding yeasts are unicellular fungi with > 1,000 known species They have evolved over a period of 400 million years and are widely distributed across different ecosystems (Walker, 2009). These yeast species have numerous traits that are of interest for life science, making them efficient cell factories to produce valuable products (Nielsen, 2019) and model organisms to study human diseases (Poswal & Saini, 2017). Subpathway evolution encompassing the discrete gene evolution events could play a significant role in gain of new functions for yeasts (Wong & Wolfe, 2005; Goncalves & Goncalves, 2019) These studies demonstrate that the evolution from gene to pathways all potentially assure that the strains have the flexibility to gain new capabilities under specific niches
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