Department of Biomolecular Chemistry, Leibniz Institute for Natural Product Research and Infection Biology (HKI), Jena 07745, Germany.
Nature. 2013 Oct 3;502(7469):124-8. doi: 10.1038/nature12588. Epub 2013 Sep 18.
Bacteria use modular polyketide synthases (PKSs) to assemble complex polyketides, many of which are leads for the development of clinical drugs, in particular anti-infectives and anti-tumoral agents. Because these multifarious compounds are notoriously difficult to synthesize, they are usually produced by microbial fermentation. During the past two decades, an impressive body of knowledge on modular PKSs has been gathered that not only provides detailed insight into the biosynthetic pathways but also allows the rational engineering of enzymatic processing lines to yield structural analogues. Notably, a hallmark of all PKS modules studied so far is the head-to-tail fusion of acyl and malonyl building blocks, which leads to linear backbones. Yet, structural diversity is limited by this uniform assembly mode. Here we demonstrate a new type of PKS module from the endofungal bacterium Burkholderia rhizoxinica that catalyses a Michael-type acetyl addition to generate a branch in the carbon chain. In vitro reconstitution of the entire PKS module, X-ray structures of a ketosynthase-branching didomain and mutagenesis experiments revealed a crucial role of the ketosynthase domain in branching the carbon chain. We present a trapped intermediary state in which acyl carrier protein and ketosynthase are covalently linked by the branched polyketide and suggest a new mechanism for chain alkylation, which is functionally distinct from terpenoid-like β-branching. For the rice seedling blight toxin rhizoxin, one of the strongest known anti-mitotic agents, the non-canonical polyketide modification is indispensable for phytotoxic and anti-tumoral activities. We propose that the formation of related pharmacophoric groups follows the same general scheme and infer a unifying vinylogous branching reaction for PKS modules with a ketosynthase-branching-acyl-carrier-protein architecture. This study unveils the structure and function of a new PKS module that broadens the biosynthetic scope of polyketide biosynthesis and sets the stage for rationally creating structural diversity.
细菌使用模块化聚酮合酶(PKS)来组装复杂的聚酮,其中许多都是开发临床药物的先导化合物,特别是抗感染和抗肿瘤药物。由于这些多种多样的化合物很难合成,因此它们通常通过微生物发酵生产。在过去的二十年中,人们积累了大量关于模块化 PKS 的知识,这些知识不仅提供了对生物合成途径的详细了解,还允许对酶处理线进行合理的工程设计以产生结构类似物。值得注意的是,迄今为止研究的所有 PKS 模块的一个特点是酰基和丙二酰基构建块的头尾融合,这导致了线性骨架。然而,这种统一的组装模式限制了结构的多样性。在这里,我们展示了一种来自内生真菌伯克霍尔德氏菌的新型 PKS 模块,该模块催化迈克尔型乙酰化反应,在碳链中产生支链。整个 PKS 模块的体外重建、酮合酶-支化双结构域的 X 射线结构和突变实验揭示了酮合酶结构域在支化碳链中的关键作用。我们提出了一个被捕获的中间状态,其中酰基载体蛋白和酮合酶通过支化聚酮共价连接,并提出了一种新的链烷基化机制,该机制在功能上与萜烯样β支化不同。对于水稻幼苗枯萎毒素根霉毒素,这是已知最强的抗有丝分裂剂之一,非典型聚酮修饰对于植物毒性和抗肿瘤活性是必不可少的。我们提出,相关药效团的形成遵循相同的一般方案,并推断出具有酮合酶-支化-酰基载体蛋白结构的 PKS 模块的统一乙烯基支化反应。这项研究揭示了一种新的 PKS 模块的结构和功能,该模块拓宽了聚酮生物合成的生物合成范围,并为合理创造结构多样性奠定了基础。