Alligamycin A, an antifungal β-lactone spiroketal macrolide from Streptomyces iranensis

Nat Commun. 2024 Oct 26;15(1):9259. doi: 10.1038/s41467-024-53695-3.

Abstract

Fungal infections pose a great threat to public health and there are only four main types of antifungal drugs, which are often limited with toxicity, drug-drug interactions and antibiotic resistance. Streptomyces is an important source of antibiotics, represented by the clinical drug amphotericin B. Here we report the discovery of alligamycin A (1) as an antifungal compound from the rapamycin-producer Streptomyces iranensis through genome-mining, genetics and natural product chemistry approaches. Alligamycin A harbors a unique chemical scaffold with 13 chiral centers, featuring a β-lactone moiety, a [6,6]-spiroketal ring, and an unreported 7-oxo-octylmalonyl-CoA extender unit incorporated by a potential crotonyl-CoA carboxylase/reductase. It is biosynthesized by a type I polyketide synthase which is confirmed through CRISPR-based gene editing. Alligamycin A displayed potent antifungal effects against numerous clinically relevant filamentous fungi, including resistant Aspergillus and Talaromyces species. β-Lactone ring is essential for the antifungal activity since alligamycin B (2) with disruption in the ring abolished the antifungal effect. Proteomics analysis revealed alligamycin A potentially disrupts the integrity of fungal cell walls and induces the expression of stress-response proteins in Aspergillus niger. Discovery of the potent antifungal candidate alligamycin A expands the limited antifungal chemical space.

MeSH terms

  • Animals
  • Antifungal Agents* / chemistry
  • Antifungal Agents* / pharmacology
  • Furans
  • Gene Editing
  • Lactones* / chemistry
  • Lactones* / metabolism
  • Lactones* / pharmacology
  • Macrolides* / chemistry
  • Macrolides* / metabolism
  • Macrolides* / pharmacology
  • Microbial Sensitivity Tests
  • Polyketide Synthases / genetics
  • Polyketide Synthases / metabolism
  • Spiro Compounds / chemistry
  • Spiro Compounds / pharmacology
  • Streptomyces* / genetics
  • Streptomyces* / metabolism

Substances

  • Antifungal Agents
  • Macrolides
  • Lactones
  • Polyketide Synthases
  • Spiro Compounds
  • spiroketal
  • Furans