SPI-1 virulence gene expression modulates motility of Salmonella Typhimurium 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 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.

Salmonella pathogenicity island-14 is a critical virulence factor responsible for systemic infection in chickens caused by Salmonella gallinarum

“…The SPI-14 gene cluster has been identified as crucial for SPI-1 expression. SPI-1 and SPI-2 in both S. enteritidis and S. typhimurium encode the Type III Secretion System (T3SS), playing a pivotal role in cell invasion and intracellular survival within the host’s intestinal tract ( 29 , 31 , 32 ). Some SPIs are ubiquitous and distributed among all Salmonella species, while other SPIs may be associated with specific serotypes, revealing adaptive advantages and host specificity ( 10 , 24 ).…”

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.…”