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

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 results in a SPI-1-dependent induction of the stringent response and a pronounced decrease of proton motive force (PMF), while flagellation was not affected. We further found that activation of HilD enhanced the adhesion of Salmonella to epithelial cells. A transcriptome analysis revealed a concomitant upregulation of several adhesin systems, which when overproduced, phenocopied the HilD-induced motility defect. We propose that a combination of SPI-1-dependent depletion of the PMF and upregulation of adhesins upon HilD-activation allows flagellated Salmonella to rapidly modulate their motility during infection, thereby enabling efficient adhesion to host cells and delivery of effector proteins.

Critical concentration of formate governs the expression of the flagellar and the pathogenicity island-1 genes inSalmonellaTyphimurium

“…Moreover, a latest study by Saleh et al have shown that HilD activation can trigger a SPI-1 dependent induction of the stringent response and considerable decrease in the Proton Motive Force (PMF). Although flagellation was unaffected, HilD-induction produced motility defect in S. Typhimurium (80).…”

“…Although flagellation was unaffected, HilD-induction produced motility defect in S . Typhimurium (80). All these studies have shown that Salmonella can modulate between its flagella synthesis and SPI-1 gene expression to achieve efficient adhesion and delivery of SPI-1 effectors.…”

Molecular characterization of virulence and resistance genes in Salmonella strains isolated from chickens sold at the informal chicken market in Gauteng Province, South Africa

“…The pathogenicity of Salmonella strains has been related to numerous virulence genes present in chromosomal Salmonella pathogenicity islands (SPIs) (Lerminiaux et al, 2020; Rodriquez‐Riviera et al, 2015; Sırıken, 2013). These virulence genes may be encoded in Salmonella pathogenicity islands and the high pathogenicity island (HPI); mobile genetic elements like virulence plasmids and bacteriophages, as well as genes encoding fimbriae, flagella, and toxins (Jiao et al, 2020; McMillan et al, 2020; Saleh et al, 2023; Wang, Wang, et al, 2020). Virulence genes encoded in SPI‐1 to SPI‐5, detection frequency, and their activities in the pathogenicity of Salmonella spp.…”