Expanded metabolic networks combined with accelerated protein evolution has enabled new cellular traits within yeast subphylum

Novel traits arise from genome evolution, but it remains ambiguous which evolutionary events modulate trait diversity in yeast subphylum. Here, we performed a multi-dimensional evolution analysis to investigate the general mechanism shaping yeast phenome diversity. We reconstructed genome-scale metabolic models for 332 yeast species to characterize versatile metabolic functions. Subsequent model simulation and selection analysis indicate that most genes are negatively selected across species, while the evolution rate of gene and codon are pathway- and function-dependent. Maping expanded and horizontal transferred genes onto pathways verify that the extended metabolic network through gene duplication and enzyme promiscuity are prominent mechanism for innovations in substrates utilization. We further find that the positive selection on multiple genes, converging on EMP pathway, contribute to the formation of more complex traits, i.e., thermotolerance and Crabtree-effect. Our findings testify that for phenotypic diversification, multi-dimensional evolution from both metabolic network structure and individual protein elements are crucial.

新性状起源于基因组演化，但目前仍无法明确哪些演化事件调控了酵母亚门的性状多样性。本研究开展多维演化分析，以探究塑造酵母表型组（phenome）多样性的通用机制。我们为332个酵母物种重建了基因组规模代谢模型（genome-scale metabolic models），以表征其多样的代谢功能。后续的模型模拟与选择分析显示，多数基因在各物种中均处于负选择状态，而基因与密码子的演化速率则与其所参与的代谢通路及功能密切相关。将扩增基因与水平转移基因映射至代谢通路后，分析结果证实，通过基因复制与酶混杂性拓展的代谢网络，是底物利用能力创新的关键机制。我们进一步发现，多个受正选择的基因汇聚于EMP途径（EMP pathway），这些基因的适应性演化推动了更复杂性状的形成，例如耐热性与克拉布特里效应（Crabtree-effect）。本研究结果证实，对于表型多样化而言，同时从代谢网络结构与单个蛋白质元件层面展开的多维演化分析至关重要。