Inhibitory effects of citral on the production of virulence factors in Staphylococcus aureus and its potential application in meat preservation

Int J Food Microbiol. 2024 Mar 2:413:110581. doi: 10.1016/j.ijfoodmicro.2024.110581. Epub 2024 Jan 18.

Abstract

Foodborne diseases caused by Staphylococcus aureus contamination on meat and meat products has gained increasing attention in recent years, while the pathogenicity of S. aureus is mainly attributed to its virulence factors production, which is primarily regulated by quorum sensing (QS) system. Herein, we aimed to uncover the inhibitory effects and mechanisms of citral (CIT) on virulence factors production by S. aureus, and further explore its potential application in pork preservation. Susceptibility test confirmed the antibacterial properties of CIT against S. aureus, the minimal inhibitory concentration (MIC) was 0.25 mg/mL. Treatment with sub-MICs of CIT reduced the hemolytic activity by inhibiting the production of α-hemolysin, and staphylococcal enterotoxins (SEs) production was significantly inhibited by CIT in both culture medium and pork without affecting bacterial growth. Transcriptomic analysis indicated that the differentially expression genes encoding α-hemolysin, SEs, and other virulence factors were down-regulated after treatment with 1/2MIC CIT. Moreover, the genes related to QS including agrA and agrC were also down-regulated, while the global transcriptional regulator sarA was up-regulated. Data here demonstrated that CIT could inhibited S. aureus virulence factors production through disturbing QS systems. In a challenge test, the addition of CIT caused a remarkable inhibition of S. aureus population and delay in lipid oxidation and color change on pork after 15 days incubation at 4 °C. These findings demonstrated that CIT could not only efficiently restrain the production of S. aureus virulence factors by disturbing QS, but also exhibit the potential application on the preservation of meat products.

Keywords: Citral; Pork preservation; Quorum sensing; Staphylococcus aureus; Virulence factor.

MeSH terms

  • Acyclic Monoterpenes*
  • Anti-Bacterial Agents / metabolism
  • Anti-Bacterial Agents / pharmacology
  • Bacterial Proteins / metabolism
  • Enterotoxins / metabolism
  • Hemolysin Proteins
  • Humans
  • Meat
  • Staphylococcal Infections* / microbiology
  • Staphylococcus aureus*
  • Virulence Factors / genetics
  • Virulence Factors / metabolism

Substances

  • Virulence Factors
  • Hemolysin Proteins
  • citral
  • Bacterial Proteins
  • Enterotoxins
  • Anti-Bacterial Agents
  • Acyclic Monoterpenes