Ekkers David M, Tusso Sergio, Moreno-Gamez Stefany, Rillo Marina C, Kuipers Oscar P, van Doorn G Sander
Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Nijenborgh 7, 9747 AG, Groningen, The Netherlands.
Molecular Genetics Group, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Nijenborgh 7, 9747 AG, Groningen, The Netherlands.
Mol Biol Evol. 2022 Jun 9;39(6). doi: 10.1093/molbev/msac124.
Mitigating trade-offs between different resource-utilization functions is key to an organism's ecological and evolutionary success. These trade-offs often reflect metabolic constraints with a complex molecular underpinning; therefore, their consequences for evolutionary processes have remained elusive. Here, we investigate how metabolic architecture induces resource utilization constraints and how these constraints, in turn, elicit evolutionary specialization and diversification. Guided by the metabolic network structure of the bacterium Lactococcus cremoris, we selected two carbon sources (fructose and galactose) with predicted co-utilization constraints. By evolving L. cremoris on either fructose, galactose or a mix of both sugars, we imposed selection favoring divergent metabolic specializations or co-utilization of both resources, respectively. Phenotypic characterization revealed the evolution of either fructose or galactose specialists in the single-sugar treatments. In the mixed sugar regime, we observed adaptive diversification: both specialists coexisted, and no generalist evolved. Divergence from the ancestral phenotype occurred at key pathway junctions in the central carbon metabolism. Fructose specialists evolved mutations in the fbp and pfk genes that appear to balance anabolic and catabolic carbon fluxes. Galactose specialists evolved increased expression of pgmA (the primary metabolic bottleneck of galactose metabolism) and silencing of ptnABCD (the main glucose transporter) and ldh (regulator/enzyme of downstream carbon metabolism). Overall, our study shows how metabolic network architecture and historical contingency serve to predict targets of selection and inform the functional interpretation of evolved mutations. The elucidation of the relationship between molecular constraints and phenotypic trade-offs contributes to an integrative understanding of evolutionary specialization and diversification.
减轻不同资源利用功能之间的权衡是生物体生态和进化成功的关键。这些权衡往往反映了具有复杂分子基础的代谢限制；因此，它们对进化过程的影响仍然难以捉摸。在这里，我们研究代谢结构如何诱导资源利用限制，以及这些限制如何反过来引发进化特化和多样化。以乳酸乳球菌的代谢网络结构为指导，我们选择了两种具有预测共利用限制的碳源（果糖和半乳糖）。通过让乳酸乳球菌在果糖、半乳糖或两种糖的混合物上进化，我们分别施加了有利于不同代谢特化或两种资源共利用的选择。表型特征揭示了在单糖处理中果糖或半乳糖特化菌的进化。在混合糖环境中，我们观察到了适应性多样化：两种特化菌共存，没有产生通才。与祖先表型的差异发生在中心碳代谢的关键途径节点上。果糖特化菌在fbp和pfk基因中发生了突变，这些突变似乎平衡了合成代谢和分解代谢的碳通量。半乳糖特化菌进化出pgmA（半乳糖代谢的主要代谢瓶颈）表达增加，以及ptnABCD（主要葡萄糖转运蛋白）和ldh（下游碳代谢的调节因子/酶）沉默。总体而言，我们的研究表明代谢网络结构和历史偶然性如何用于预测选择目标，并为进化突变的功能解释提供信息。阐明分子限制与表型权衡之间的关系有助于对进化特化和多样化进行综合理解。
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