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<p>Self-aggregation into biofilms is a bacterial stress response that promotes antimicrobial resistance because biofilms comprise viscous extracellular polymeric matrices that impede antimicrobial diffusion. Extracellular DNA (eDNA) is typically a principal component of the biofilm matrix. Here we show that persistent R-loops, which are three-stranded nucleic acid structures consisting of single DNA and a DNA:RNA hybrid, contribute to the viscoelastic behaviour of eDNA in <i>Pseudomonas aeruginosa</i> biofilms. The RNA strands are inserted throughout the genome by the strand exchange protein RecA, at locations in the genome distant from the site of their own transcription i.e. in <i>trans</i>. R-loop formation creates genomic instability in bacterial cells that subsequently die and release R-loops. These events appear to occur as part of a programmed cell death pathway, which is activated by the stringent stress response. The released R-loops become building blocks of the viscoelastic extracellular matrix, for the benefit of the remaining population. Our results indicate that R-loops facilitate the formation of the viscoelastic eDNA matrix in the context of bacterial stress responses, and that interfering with the R-loops may provide a broadly effective strategy for biofilm control.</p>

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Stress-induced toxic genomic R-loops support biofilm extracellular matrix formation

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2025年12月12日

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  • Sudarsan Mugunthan,
  • Zhang Dong,
  • Sanjay H. Chotirmall,
  • Staffan Kjelleberg,
  • Thomas Seviour

摘要

Self-aggregation into biofilms is a bacterial stress response that promotes antimicrobial resistance because biofilms comprise viscous extracellular polymeric matrices that impede antimicrobial diffusion. Extracellular DNA (eDNA) is typically a principal component of the biofilm matrix. Here we show that persistent R-loops, which are three-stranded nucleic acid structures consisting of single DNA and a DNA:RNA hybrid, contribute to the viscoelastic behaviour of eDNA in Pseudomonas aeruginosa biofilms. The RNA strands are inserted throughout the genome by the strand exchange protein RecA, at locations in the genome distant from the site of their own transcription i.e. in trans. R-loop formation creates genomic instability in bacterial cells that subsequently die and release R-loops. These events appear to occur as part of a programmed cell death pathway, which is activated by the stringent stress response. The released R-loops become building blocks of the viscoelastic extracellular matrix, for the benefit of the remaining population. Our results indicate that R-loops facilitate the formation of the viscoelastic eDNA matrix in the context of bacterial stress responses, and that interfering with the R-loops may provide a broadly effective strategy for biofilm control.