Dabos Laura, Nedjari Inssaf, Couce Alejandro
Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Madrid, Spain.
Laboratoire de Physique de l'Ecole Normale Supérieure, Université PSL, Sorbonne Université, Université Paris Cité and CNRS, Paris, France.
Nat Ecol Evol. 2025 Jul 30. doi: 10.1038/s41559-025-02804-6.
Interactions among beneficial mutations (that is, epistasis) are often strong enough to direct adaptation through alternative mutational paths. Although alternative solutions should display similar fitness under the primary selective conditions, their properties across secondary environments may differ widely. The extent to which these cryptic differences are to be expected is largely unknown, despite their importance-for example, in identifying exploitable collateral sensitivities among mutations conferring antibiotic resistance. Here we use directed evolution to characterize the diversity of mutational paths through which the prevalent carbapenemase Klebsiella pneumoniae carbapenemase-2 can evolve high activity against the clinically relevant antibiotic ceftazidime, an initially poor substrate. We identified 40 different substitutions-including many that are common in clinical settings-spread among 18 different mutational trajectories. Initial mutations determined four major groups into which the trajectories can be classified, a signature of strong epistasis. Despite similar final ceftazidime resistance, groups diverged markedly across multiple phenotypic dimensions, from molecular traits, such as in-cell stability and catalytic efficiency, to macroscopic traits, such as growth rate and activity against other β-lactam antibiotics. Our results indicate that cryptic yet consequential phenotypic differences can accumulate rapidly under strong selection, unpredictably shaping the long-term success of resistance enzymes in their journey across hosts and environments.
有益突变之间的相互作用(即上位性)通常很强,足以通过替代突变路径引导适应性进化。尽管在主要选择条件下,替代解决方案应表现出相似的适应性,但它们在次要环境中的特性可能差异很大。尽管这些隐秘差异很重要,例如在识别赋予抗生素抗性的突变之间可利用的间接敏感性方面,但人们对预期出现这些差异的程度知之甚少。在这里,我们使用定向进化来表征常见碳青霉烯酶肺炎克雷伯菌碳青霉烯酶-2(Klebsiella pneumoniae carbapenemase-2)针对临床相关抗生素头孢他啶(一种最初较差的底物)进化出高活性的突变路径的多样性。我们鉴定出40种不同的取代——包括许多在临床环境中常见的取代——分布在18条不同的突变轨迹中。初始突变决定了轨迹可分为的四个主要组,这是强上位性的一个特征。尽管最终对头孢他啶的抗性相似,但这些组在多个表型维度上存在明显差异,从分子特征,如细胞内稳定性和催化效率,到宏观特征,如生长速率和对其他β-内酰胺抗生素的活性。我们的结果表明,在强烈选择下,隐秘但具有重要影响的表型差异可能会迅速积累,不可预测地塑造抗性酶在跨越宿主和环境过程中的长期成功。