The Number and Type of Chaperone-Usher Fimbriae Reflect Phylogenetic Clade Rather than Host Range in Salmonella

Salmonella is one of the most successful foodborne pathogens worldwide, owing in part to its ability to colonize or infect a wide range of hosts. Salmonella serovars are known to encode a variety of different fimbriae (hairlike organelles that facilitate binding to surfaces); however, the distribution, number, and sequence diversity of fimbriae encoded across different lineages of Salmonella were unknown. We queried whole-genome sequence (WGS) data for 242 Salmonella enterica subsp. enterica (subspecies enterica) isolates from the top 217 serovars associated with isolation from humans and agricultural animals; this effort identified 2,894 chaperone-usher (CU)-type fimbrial usher sequences, representing the most conserved component of CU fimbriae. On average, isolates encoded 12 different CU fimbrial ushers (6 to 18 per genome), although the distribution varied significantly (P = 1.328E−08) by phylogenetic clade, with isolates in section Typhi having significantly fewer fimbrial ushers than isolates in clade A2 (medians = 10 and 12 ushers, respectively). Characterization of fimbriae in additional non-enterica subspecies genomes suggested that 8 fimbrial ushers were classified as being unique to subspecies enterica isolates, suggesting that the majority of fimbriae were most likely acquired prior to the divergence of subspecies enterica. Characterization of mobile elements suggested that plasmids represent an important vehicle facilitating the acquisition of a wide range of fimbrial ushers, particularly for the acquisition of fimbriae from other Gram-negative genera. Overall, our results suggest that differences in the number and type of fimbriae encoded most likely reflect differences in phylogenetic clade rather than differences in host range. IMPORTANCE Fimbriae of the CU assembly pathway represent important organelles that mediate Salmonella’s interactions with host tissues and abiotic surfaces. Our analyses provide a comprehensive overview of the diversity of CU fimbriae in Salmonella spp., highlighting that the majority of CU fimbriae are distributed broadly across multiple subspecies and suggesting that acquisition most likely occurred prior to the divergence of subspecies enterica. Our data also suggest that plasmids represent the primary vehicles facilitating the horizontal transfer of diverse CU fimbriae in Salmonella. Finally, the observed high sequence similarity between some ushers suggests that different names may have been assigned to closely related fimbrial ushers that likely should be represented by a single designation. This highlights the need to establish standard criteria for fimbria classification and nomenclature, which will also facilitate future studies seeking to associate virulence factors with adaptation to or differences in the likelihood of causing disease in a given host.