Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA.
Microbial Sciences Institute, Yale University, New Haven, CT, USA.
Mol Biol Evol. 2023 Sep 1;40(9). doi: 10.1093/molbev/msad187.
Microbial strategies for resource use are an essential determinant of their fitness in complex habitats. When facing environments with multiple nutrients, microbes often use them sequentially according to a preference hierarchy, resulting in well-known patterns of diauxic growth. In theory, the evolutionary diversification of metabolic hierarchies could represent a mechanism supporting coexistence and biodiversity by enabling temporal segregation of niches. Despite this ecologically critical role, the extent to which substrate preference hierarchies can evolve and diversify remains largely unexplored. Here, we used genome-scale metabolic modeling to systematically explore the evolution of metabolic hierarchies across a vast space of metabolic network genotypes. We find that only a limited number of metabolic hierarchies can readily evolve, corresponding to the most commonly observed hierarchies in genome-derived models. We further show how the evolution of novel hierarchies is constrained by the architecture of central metabolism, which determines both the propensity to change ranks between pairs of substrates and the effect of specific reactions on hierarchy evolution. Our analysis sheds light on the genetic and mechanistic determinants of microbial metabolic hierarchies, opening new research avenues to understand their evolution, evolvability, and ecology.
微生物利用资源的策略是其在复杂生境中适应能力的重要决定因素。当面临多种营养物质的环境时，微生物通常会根据优先层次顺序使用它们，从而产生众所周知的双相生长模式。从理论上讲，代谢层次结构的进化多样化可能是通过使生态位时间隔离来支持共存和生物多样性的一种机制。尽管这种生态作用至关重要，但底物偏好层次结构进化和多样化的程度在很大程度上仍未得到探索。在这里，我们使用基因组规模的代谢建模来系统地探索代谢网络基因型广阔空间中代谢层次结构的进化。我们发现，只有少数代谢层次结构可以轻易进化，这与从基因组衍生的模型中最常见的层次结构相对应。我们进一步展示了新层次结构的进化如何受到中心代谢的结构限制，这决定了两对底物之间改变等级的倾向以及特定反应对层次结构进化的影响。我们的分析揭示了微生物代谢层次结构的遗传和机制决定因素，为理解它们的进化、可进化性和生态学开辟了新的研究途径。
