An inhibitory mechanism of AasS, an exogenous fatty acid scavenger: Implications for re-sensitization of FAS II antimicrobials

PLoS Pathog. 2024 Jul 15;20(7):e1012376. doi: 10.1371/journal.ppat.1012376. eCollection 2024 Jul.

Abstract

Antimicrobial resistance is an ongoing "one health" challenge of global concern. The acyl-ACP synthetase (termed AasS) of the zoonotic pathogen Vibrio harveyi recycles exogenous fatty acid (eFA), bypassing the requirement of type II fatty acid synthesis (FAS II), a druggable pathway. A growing body of bacterial AasS-type isoenzymes compromises the clinical efficacy of FAS II-directed antimicrobials, like cerulenin. Very recently, an acyl adenylate mimic, C10-AMS, was proposed as a lead compound against AasS activity. However, the underlying mechanism remains poorly understood. Here we present two high-resolution cryo-EM structures of AasS liganded with C10-AMS inhibitor (2.33 Å) and C10-AMP intermediate (2.19 Å) in addition to its apo form (2.53 Å). Apart from our measurements for C10-AMS' Ki value of around 0.6 μM, structural and functional analyses explained how this inhibitor interacts with AasS enzyme. Unlike an open state of AasS, ready for C10-AMP formation, a closed conformation is trapped by the C10-AMS inhibitor. Tight binding of C10-AMS blocks fatty acyl substrate entry, and therefore inhibits AasS action. Additionally, this intermediate analog C10-AMS appears to be a mixed-type AasS inhibitor. In summary, our results provide the proof of principle that inhibiting salvage of eFA by AasS reverses the FAS II bypass. This facilitates the development of next-generation anti-bacterial therapeutics, esp. the dual therapy consisting of C10-AMS scaffold derivatives combined with certain FAS II inhibitors.

MeSH terms

  • Anti-Bacterial Agents / pharmacology
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / metabolism
  • Coenzyme A Ligases / antagonists & inhibitors
  • Coenzyme A Ligases / metabolism
  • Cryoelectron Microscopy
  • Fatty Acid Synthase, Type II / antagonists & inhibitors
  • Fatty Acid Synthase, Type II / metabolism
  • Fatty Acids* / chemistry
  • Fatty Acids* / metabolism
  • Vibrio* / drug effects

Substances

  • Fatty Acids
  • Bacterial Proteins
  • Anti-Bacterial Agents
  • Coenzyme A Ligases
  • Fatty Acid Synthase, Type II

Supplementary concepts

  • Vibrio harveyi

Grants and funding

This work was supported by National Natural Science Foundation of China (32141001 & 31830001, YF), National Science Fund for Distinguished Young Scholar (32125003, YF), and National Key Research & Development Program of China (2023YFC2307100 & 2023YFC2300021, YF). The funders play no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.