Allicin, a natural antimicrobial defence substance from garlic, inhibits DNA gyrase activity in bacteria

Int J Med Microbiol. 2020 Jan;310(1):151359. doi: 10.1016/j.ijmm.2019.151359. Epub 2019 Sep 25.

Abstract

Allicin (diallylthiosulfinate) is a potent antimicrobial substance, produced by garlic tissues upon wounding as a defence against pathogens and pests. Allicin is a reactive sulfur species (RSS) that oxidizes accessible cysteines in glutathione and proteins. We used a differential isotopic labelling method (OxICAT) to identify allicin targets in the bacterial proteome. We compared the proteomes of allicin-susceptible Pseudomonas fluorescens Pf0-1 and allicin-tolerant PfAR-1 after a sublethal allicin exposure. Before exposure to allicin, proteins were in a predominantly reduced state, with approximately 77% of proteins showing less than 20% cysteine oxidation. Protein oxidation increased after exposure to allicin, and only 50% of proteins from allicin-susceptible Pf0-1, but 65% from allicin-tolerant PfAR-1, remained less than 20% oxidised. DNA gyrase was identified as an allicin target. Cys433 in DNA gyrase subunit A (GyrA) was approximately 6% oxidized in untreated bacteria. After allicin treatment the degree of Cys433 oxidation increased to 55% in susceptible Pf0-1 but only to 10% in tolerant PfAR-1. Allicin inhibited E. coli DNA gyrase activity in vitro in the same concentration range as nalidixic acid. Purified PfAR-1 DNA gyrase was inhibited to greater extent by allicin in vitro than the Pf0-1 enzyme. Substituting PfAR-1 GyrA into Pf0-1 rendered the exchange mutants more susceptible to allicin than the Pf0-1 wild type. Taken together, these results suggest that GyrA was protected from oxidation in vivo in the allicin-tolerant PfAR-1 background, rather than the PfAR-1 GyrA subunit being intrinsically less susceptible to oxidation by allicin than the Pf0-1 GyrA subunit. DNA gyrase is a target for medicinally important antibiotics; thus, allicin and its analogues may have potential to be developed as gyrase inhibitors, either alone or in conjunction with other therapeutics.

Keywords: Allicin; Antimicrobial; DNA gyrase; Garlic; GyrA; Pseudomonas.

MeSH terms

  • Anti-Bacterial Agents / pharmacology*
  • Bacteria / drug effects*
  • Bacteria / enzymology
  • Cysteine / metabolism
  • DNA Gyrase / genetics
  • DNA Gyrase / metabolism*
  • Disulfides
  • Escherichia coli / drug effects
  • Escherichia coli / enzymology
  • Garlic / chemistry*
  • Oxidation-Reduction
  • Proteome
  • Pseudomonas fluorescens / drug effects
  • Sulfinic Acids / pharmacology*
  • Topoisomerase II Inhibitors / pharmacology*

Substances

  • Anti-Bacterial Agents
  • Disulfides
  • Proteome
  • Sulfinic Acids
  • Topoisomerase II Inhibitors
  • allicin
  • DNA Gyrase
  • Cysteine