Two-component system RstAB promotes the pathogenicity of adherent-invasive Escherichia coli in response to acidic conditions within macrophages

Gut Microbes. 2024 Jan-Dec;16(1):2356642. doi: 10.1080/19490976.2024.2356642. Epub 2024 May 20.

Abstract

Adherent-invasive Escherichia coli (AIEC) strain LF82, isolated from patients with Crohn's disease, invades gut epithelial cells, and replicates in macrophages contributing to chronic inflammation. In this study, we found that RstAB contributing to the colonization of LF82 in a mouse model of chronic colitis by promoting bacterial replication in macrophages. By comparing the transcriptomes of rstAB mutant- and wild-type when infected macrophages, 83 significant differentially expressed genes in LF82 were identified. And we identified two possible RstA target genes (csgD and asr) among the differentially expressed genes. The electrophoretic mobility shift assay and quantitative real-time PCR confirmed that RstA binds to the promoters of csgD and asr and activates their expression. csgD deletion attenuated LF82 intracellular biofilm formation, and asr deletion reduced acid tolerance compared with the wild-type. Acidic pH was shown by quantitative real-time PCR to be the signal sensed by RstAB to activate the expression of csgD and asr. We uncovered a signal transduction pathway whereby LF82, in response to the acidic environment within macrophages, activates transcription of the csgD to promote biofilm formation, and activates transcription of the asr to promote acid tolerance, promoting its replication within macrophages and colonization of the intestine. This finding deepens our understanding of the LF82 replication regulation mechanism in macrophages and offers new perspectives for further studies on AIEC virulence mechanisms.

Keywords: Adherent-invasive Escherichia coli (AIEC); RstAB; acid; asr; biofilm; csgD; macrophages.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acids / metabolism
  • Animals
  • Bacterial Adhesion*
  • Biofilms* / growth & development
  • Colitis / microbiology
  • Crohn Disease / microbiology
  • Disease Models, Animal
  • Escherichia coli Infections* / microbiology
  • Escherichia coli Proteins* / genetics
  • Escherichia coli Proteins* / metabolism
  • Escherichia coli* / genetics
  • Escherichia coli* / metabolism
  • Escherichia coli* / pathogenicity
  • Gene Expression Regulation, Bacterial*
  • Humans
  • Hydrogen-Ion Concentration
  • Macrophages* / microbiology
  • Mice
  • Signal Transduction
  • Virulence

Grants and funding

This work was supported by the National Natural Science Foundation of China Program under Grant [Grant No. 32100144 and 32270191], the China Postdoctoral Science Foundation Program under Grant [Grant No. 2020M670623], the Fundamental Research Funds for the Central Universities, Nankai University [Grant No. 63233172], and the Fundamental Research Funds for the Central Universities [Grant No. 63241467].