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Directed Evolution of Adenylation-Domains Guided by Hydroxamate Profiling (DEHAMA)

Subject Area Biological and Biomimetic Chemistry
Term from 2020 to 2024
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 441781663
 
Final Report Year 2024

Final Report Abstract

Nonribosomal peptide synthetases (NRPSs) are enzymes involved in the production of multifarious bioactive natural products, such as ciclosporin, vancomycin and surfactin. Through NRPS engineering, these compounds can potentially be structurally diversified and tailored to certain applications. To this end we have developed an engineering workflow to broaden the substrate spectrum of the adenylation (A-) domain which is primarily responsible for substrate selection in NRPSs. This workflow is based on the hypothesis that promiscuous enzymes are versatile evolutionary intermediates in nature and in the lab. We have mutated the A-domain in module SrfAC from surfactin biosynthesis while monitoring the full substrate spectrum of hundreds of mutants via hydroxamate profiling (HAMA). HAMA disentangles by mass spectrometry which hydroxamate products are formed when the quencher hydroxylamine is added to an A-domain reaction. With HAMA, dozens of substrates can be tested in parallel which reflects the situation inside a cell and yields a comprehensive specificity profile of an A-domain in a single experiment. Converting SrfAC into the highly promiscuous “SrfA- Chub” - a versatile hub to reach various specificities - has been performed by applying the computational tool FuncLib which predicts diversified protein sequences that also remain functional. Based on HAMA profiles of mutational libraries constructed in the process, we have quantified the influence of individual A-domain residues on specificity to inform future directed evolution experiments. The promiscuous SrfAChub provides an artificial model of a promiscuous evolutionary intermediate and its characterization contributes to our understanding of natural NRPS evolution. Our strategy will also provide a blueprint to enhance promiscuity in related A-domains, so that structural variations can be introduced into bioactive nonribosomal peptides in a more streamlined fashion. Altogether, these experiments have advanced our understanding of NRPS engineering and evolution, thus laying the basis for tailoring the biosynthesis of life-saving peptide drugs in the future.

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