Small RNA OxyS induces resistance to aminoglycosides during oxidative stress by controlling Fe-S cluster biogenesis in Escherichia coli

Proc Natl Acad Sci U S A. 2024 Nov 12;121(46):e2317858121. doi: 10.1073/pnas.2317858121. Epub 2024 Nov 4.

Abstract

Fe-S clusters are essential cofactors involved in many reactions across all domains of life. Their biogenesis in Escherichia coli and other enterobacteria involves two machineries: Isc and Suf. Under conditions where cells operate with the Suf system, such as during oxidative stress or iron limitation, the entry of aminoglycosides is reduced, leading to resistance to these antibiotics. The transition between Isc and Suf machineries is controlled by the transcriptional regulator IscR. Here, we found that two small regulatory RNAs (sRNAs), FnrS and OxyS, control iscR expression by base pairing to the 5'-UTR of the iscR mRNA. These sRNAs act in opposite ways and in opposite conditions: FnrS, expressed in anaerobiosis, represses the expression of iscR while OxyS, expressed during oxidative stress, activates it. Using an E. coli strain experiencing protracted oxidative stress, we further demonstrate that iscR expression is rapidly and significantly enhanced in the presence of OxyS. Consequently, we further show that OxyS induces resistance to aminoglycosides during oxidative stress through regulation of Fe-S cluster biogenesis, revealing a major role for this sRNA.

Keywords: antibiotic resistance; oxidative stress; sRNAs; stress response.

MeSH terms

  • Aminoglycosides* / pharmacology
  • Anti-Bacterial Agents / pharmacology
  • Drug Resistance, Bacterial* / genetics
  • Escherichia coli Proteins* / genetics
  • Escherichia coli Proteins* / metabolism
  • Escherichia coli* / drug effects
  • Escherichia coli* / genetics
  • Escherichia coli* / metabolism
  • Gene Expression Regulation, Bacterial* / drug effects
  • Iron-Sulfur Proteins* / genetics
  • Iron-Sulfur Proteins* / metabolism
  • Oxidative Stress* / drug effects
  • RNA, Bacterial / genetics
  • RNA, Bacterial / metabolism
  • RNA, Small Untranslated / genetics
  • RNA, Small Untranslated / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Aminoglycosides
  • Escherichia coli Proteins
  • Iron-Sulfur Proteins
  • RNA, Small Untranslated
  • Anti-Bacterial Agents
  • RNA, Bacterial
  • IscR protein, E coli
  • Transcription Factors
  • FNR protein, E coli