Abstract
The speG gene has been reported to regulate polyamine metabolism in Escherichia coli and Shigella, but its role in Salmonella remains unknown. Our preliminary studies have revealed that speG widely affects the transcriptomes of infected in vitro M and Caco-2 cells and that it is required for the intracellular replication of Salmonella enterica serovar Typhimurium (S. Typhimurium) in HeLa cells. In this study, we demonstrated that speG plays a time-dependent and cell type-independent role in the intracellular replication of S. Typhimurium. Moreover, high-performance liquid chromatography (HPLC) of four major polyamines demonstrated putrescine, spermine, and cadaverine as the leading polyamines in S. Typhimurium. The deletion of speG significantly increased the levels of the three polyamines in intracellular S. Typhimurium, suggesting the inhibitory effect of speG on the biosynthesis of these polyamines. The deletion of speG was associated with elevated levels of these polyamines in the attenuated intracellular replication of S. Typhimurium in host cells. This result was subsequently validated by the dose-dependent suppression of intracellular proliferation after the addition of the polyamines. Furthermore, our RNA transcriptome analysis of S. Typhimurium SL1344 and its speG mutant outside and inside Caco-2 cells revealed that speG regulates the genes associated with flagellar biosynthesis, fimbrial expression, and functions of types III and I secretion systems. speG also affects the expression of genes that have been rarely reported to correlate with polyamine metabolism in Salmonella, including those associated with the periplasmic nitrate reductase system, glucarate metabolism, the phosphotransferase system, cytochromes, and the succinate reductase complex in S. Typhimurium in the mid-log growth phase, as well as those in the ilv–leu and histidine biosynthesis operons of intracellular S. Typhimurium after invasion in Caco-2 cells. In the present study, we characterized the phenotypes and transcriptome effects of speG in S. Typhimurium and reviewed the relevant literature to facilitate a more comprehensive understanding of the potential role of speG in the polyamine metabolism and virulence regulation of Salmonella.
Highlights
Non-typhoidal Salmonella are important pathogens that cause a wide spectrum of diseases and considerable morbidity and mortality in humans and animals worldwide (Hohmann, 2001)
Typhimurium speG was significantly attenuated in output pool B in HeLa cells at 18 h postinfection, but not in output pool A at 3 h postinfection (1.1 × 107 vs. 1.9 × 107 colony-forming units (CFU)/well, p < 0.05; Figure 1B)
According to our review of relevant literature, the present study is the first to demonstrate that speG is required for the intracellular replication of Salmonella in human non-phagocytic cells
Summary
Non-typhoidal Salmonella are important pathogens that cause a wide spectrum of diseases and considerable morbidity and mortality in humans and animals worldwide (Hohmann, 2001). Host cell invasion (Pace et al, 1993) and intracellular replication (Leung and Finlay, 1991) are essential for the pathogenesis of Salmonella enterica serovar Typhimurium The SPI-2 T3SS is essential for bacterial intracellular replication in Salmonella-containing vacuoles in host cells through the translocation of approximately 30 SPI-2 T3SS effector proteins into the host endomembrane system and cytosol (Figueira and Holden, 2012). SPI-2 T3SS genes associated with the intracellular replication of Salmonella have been mostly reported in phagocytic cells (Helaine et al, 2010; Figueira and Holden, 2012; Figueira et al, 2013). A few studies have demonstrated that SPI-1 T3SS genes are required for intracellular replication in human cervical epithelial
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