SPI-1 virulence gene expression modulates motility of Salmonella Typhimurium in a proton motive force- and adhesins-dependent manner

PLoS Pathog. 2023 Jun 14;19(6):e1011451. doi: 10.1371/journal.ppat.1011451. eCollection 2023 Jun.

Abstract

Both the bacterial flagellum and the evolutionary related injectisome encoded on the Salmonella pathogenicity island 1 (SPI-1) play crucial roles during the infection cycle of Salmonella species. The interplay of both is highlighted by the complex cross-regulation that includes transcriptional control of the flagellar master regulatory operon flhDC by HilD, the master regulator of SPI-1 gene expression. Contrary to the HilD-dependent activation of flagellar gene expression, we report here that activation of HilD resulted in a dramatic loss of motility, which was dependent on the presence of SPI-1. Single cell analyses revealed that HilD-activation triggers a SPI-1-dependent induction of the stringent response and a substantial decrease in proton motive force (PMF), while flagellation remains unaffected. We further found that HilD activation enhances the adhesion of Salmonella to epithelial cells. A transcriptome analysis revealed a simultaneous upregulation of several adhesin systems, which, when overproduced, phenocopied the HilD-induced motility defect. We propose a model where the SPI-1-dependent depletion of the PMF and the upregulation of adhesins upon HilD-activation enable flagellated Salmonella to rapidly modulate their motility during infection, thereby enabling efficient adhesion to host cells and delivery of effector proteins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Gene Expression
  • Gene Expression Regulation, Bacterial
  • Genomic Islands / genetics
  • Proton-Motive Force
  • Salmonella typhimurium*
  • Transcription Factors* / metabolism
  • Virulence / genetics

Substances

  • Transcription Factors
  • lambda Spi-1
  • Bacterial Proteins

Grants and funding

This work was supported in part by a project that has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement n° 864971) and from the VolkswagenStiftung (to M.E.) and by a GERLS scholarship (n° 91705821) co-funded by the Egyptian Ministry of Higher Education and Scientific Research (MHESR) and the German Academic Exchange Service (Deutscher Akademischer Austauschdienst (DAAD)) (to D.O.S.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.