stg fimbrial operon from S. Typhi STH2370 contributes to association and cell disruption of epithelial and macrophage-like cells

Abstract

BackgroundSalmonella enterica serovar Typhi (S. Typhi) stg operon, encoding a chaperone/usher fimbria (CU), contributes to an increased adherence to human epithelial cells. However, one report suggests that the presence of the Stg fimbria impairs the monocyte—bacteria association, as deduced by the lower level of invasion to macrophage-like cells observed when the stg fimbrial cluster was overexpressed. Nevertheless, since other CU fimbrial structures increase the entry of S. Typhi into macrophages, and considering that transcriptomic analyses revealed that stg operon is indeed expressed in macrophages, we reassessed the role of the stg operon in the interaction between S. Typhi strain STH2370 and human cells, including macrophage-like cells and mononuclear cells directly taken from human peripheral blood.ResultsWe compared S. Typhi STH2370 WT, a Chilean clinical strain, and the S. Typhi STH2370 Δstg mutant with respect to association and invasion using epithelial and macrophage-like cells. We observed that deletion of stg operon reduced the association and invasion of S. Typhi, in both cellular types. The presence of the cloned stg operon restored the WT phenotype in all the cases. Moreover, we compared Salmonella enterica sv. Typhimurium 14028s (S. Typhimurium, a serovar lacking stg operon) and S. Typhimurium heterologously expressing S. Typhi stg. We found that the latter presents an increased cell disruption of polarized epithelial cells and an increased association in both epithelial and macrophage-like cells.ConclusionsS. Typhi stg operon encodes a functional adhesin that participates in the interaction bacteria—eukaryotic cells, including epithelial cells and macrophages-like cells. The phenotypes associated to stg operon include increased association and consequent invasion in bacteria—eukaryotic cells, and cell disruption.Electronic supplementary materialThe online version of this article (doi:10.1186/s40659-015-0024-9) contains supplementary material, which is available to authorized users.

New Insights into the Roles of Long Polar Fimbriae and Stg Fimbriae in Salmonella Interactions with Enterocytes and M Cells

“…1A). Finally, expression of stg in S. Typhimurium resulted in increased adherence to Caco-2 cells, as seen previously (45), and a noticeable but nonsignificant decrease in adherence to M-like cells.…”

“…Despite the severely truncated chaperone protein, the stg operon appears to encode a functional adhesin. Strains carrying the stg operon are known to enhance S. Typhi adherence to a number of epithelial cell lines, including INT-407 cells (44), HEp2 cells, and polarized HT-29 cells (45). We have expanded these findings to include polarized Caco-2 cells.…”

“…to the presence of the Stg fimbriae/adhesin (44,45). Further, it is also likely that S. Typhimurium is more proficient than S. Typhi at colonizing Peyer's patches due, in part, to the presence of Lpf.…”

Functional Analysis of the Chaperone-Usher Fimbrial Gene Clusters of Salmonella enterica serovar Typhi

“…Typhi genome possesses a unique repertoire of 14 putative fimbrial clusters identified by whole-genome sequencing (Humphries et al, 2003 ) including 12 CU fimbriae (Townsend et al, 2001 ). However, only 3 CU fimbriae (Stg, Sta, and Tcf) were previously studied (Forest et al, 2007 ; Bishop et al, 2008 ; Berrocal et al, 2015 ; Leclerc et al, 2016 ; Gonzales et al, 2017 ), mainly due to the weak expression of most of these fimbriae under laboratory conditions (Low et al, 2006 ; De Masi et al, 2017 ). Among the CU fimbriae, 5 ( stg, sef , sta, ste , and tcf ) are present in S .…”

The Typhi colonization factor (Tcf) is encoded by multiple non-typhoidal Salmonella serovars but exhibits a varying expression profile and interchanging contribution to intestinal colonization

“…Different chaperone-usher fimbriae have been previously reported to be involved in diverse virulence-associated phenotypes including biofilm formation, macrophages uptake, host cell adhesion and invasion. [37][38][39][40] To determine the role of Tcf in NTS virulence-associated phenotypes, a null deletion of tcfABCD was constructed in the genome of clinical isolates of serovars Heidelberg, Schwarzengrund and Infantis and the potential role of Tcf in the above phenotypes was subsequently studied.…”