Multiple insertions of fimbrial operons correlate with the evolution of Salmonella serovars responsible for human disease

Abstract

On centisome 7, Salmonella spp. contain a large region not present in the corresponding region of Escherichia coli. This region is flanked by sequences with significant homology to the E. coli tRNA gene aspV and the hypothetical E. coli open reading frame yafV. The locus consists of a mosaic of differentially acquired inserts forming a dynamic cs7 region of horizontally transferred inserts. Salmonella enterica subspecies I, responsible for most Salmonella infections in warm‐blooded animals, carries a fimbrial gene cluster (saf) in this region as well as a regulatory gene (sinR). These genes are flanked by inverted repeats and are inserted in another laterally transferred region present in most members of Salmonella spp. encoding a putative invasin (pagN ). S. enterica subspecies I serovar Typhi, the Salmonella serovar that causes the most severe form of human salmonellosis, contains an additional insert of at least 8 kb in the sinR–pagN intergenic region harbouring a novel fimbrial operon (tcf ) similar to the coo operon encoding the CS1 fimbrial adhesin expressed by human‐specific enterotoxigenic E. coli. It is suggested that the multiple insertions of fimbrial genes that have occurred in the cs7 region have contributed to phylogenetic diversity and host adaptation of Salmonella spp.

Evolution of the Chaperone/Usher Assembly Pathway: Fimbrial Classification Goes Greek

“…3). Previous studies (8,102) listed ushers of Burkholderia cepacia (CblC) (282,332), E. coli (CfaC, CooC, CosC, CotC, CsaC, CsbC, CsdC, and CsuC) (7,8,97,99,100,125,164), S. enterica serotype Typhi (TcfC) (72,95), and Yersinia pestis (YPO3798) (254) as being members of the alternate chaperone/usher family. The ␣-fimbrial clade defined in this study includes additional usher proteins, one of which, CsfC (CS5 fimbriae), had not previously been classified as a member of the alternate chaperone/usher family.…”

“…The fact that all fimbrial operons of the ␣-fimbriae that are present in E. coli encode human-specific colonization factors is somewhat surprising, since it is not apparent why variants with tip adhesins that would bind receptors present in other vertebrate host species were not selected during diversification of this group. Interestingly, another member of the ␣-fimbrial clade, TcfC, is present in strictly human-adapted pathogens, including S. enterica serotype Typhi and S. enterica serotype Paratyphi A (95,217,336). However, fimbriae encoded by the chromosomally located tcf operon have not been functionally characterized.…”

The Different Strategies Used by Salmonella to Invade Host Cells

“…pagN, is localized on the centisome 7 genomic island and is widely distributed among Salmonella enterica serotypes (Folkesson et al, 1999). The pagN ORF was originally identified during a TnphoA random-insertion screening in S. Typhimurium performed to discover PhoPactivated genes (Belden & Miller, 1994).…”

Type VI Secretion System-Associated Gene Clusters Contribute to Pathogenesis of Salmonella enterica Serovar Typhimurium

“…enterica T6SS was first described as part of the S. enterica centisome 7 genomic island (SCI) as a contributing factor in eukaryotic pathogenesis (16). Aside from the T6SS, SCI also contains the adhesin and invasin PagN, the fimbrial gene cluster safABCD, and the transcriptional regulator sinR (15,26). Deletion of SCI resulted in an approximately 50% reduction in internalization of HEp-2 cells that could not be complemented by PagN expression; however, complementation with safABCD or sinR was not tested (16).…”