Citrate serves as a signal molecule to modulate carbon metabolism and iron homeostasis in Staphylococcus aureus

PLoS Pathog. 2024 Jul 30;20(7):e1012425. doi: 10.1371/journal.ppat.1012425. eCollection 2024 Jul.

Abstract

Pathogenic bacteria's metabolic adaptation for survival and proliferation within hosts is a crucial aspect of bacterial pathogenesis. Here, we demonstrate that citrate, the first intermediate of the tricarboxylic acid (TCA) cycle, plays a key role as a regulator of gene expression in Staphylococcus aureus. We show that citrate activates the transcriptional regulator CcpE and thus modulates the expression of numerous genes involved in key cellular pathways such as central carbon metabolism, iron uptake and the synthesis and export of virulence factors. Citrate can also suppress the transcriptional regulatory activity of ferric uptake regulator. Moreover, we determined that accumulated intracellular citrate, partly through the activation of CcpE, decreases the pathogenic potential of S. aureus in animal infection models. Therefore, citrate plays a pivotal role in coordinating carbon metabolism, iron homeostasis, and bacterial pathogenicity at the transcriptional level in S. aureus, going beyond its established role as a TCA cycle intermediate.

MeSH terms

  • Animals
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Carbon* / metabolism
  • Citric Acid Cycle
  • Citric Acid* / metabolism
  • Gene Expression Regulation, Bacterial*
  • Homeostasis*
  • Iron* / metabolism
  • Mice
  • Signal Transduction
  • Staphylococcal Infections* / metabolism
  • Staphylococcal Infections* / microbiology
  • Staphylococcus aureus* / genetics
  • Staphylococcus aureus* / metabolism
  • Staphylococcus aureus* / pathogenicity

Substances

  • Iron
  • Carbon
  • Citric Acid
  • Bacterial Proteins

Grants and funding

This work was supported by grants from National Key Research and Development Program of China (grant no. 2023YFD1800100 to LL), Hangzhou Institute for Advanced Study, UCAS (grant no. 2023HIAS-V006 to LL), National Natural Science Foundation of China (NSFC) (grant nos. 32270184 to LL and 31700124 to FC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.