Strain and host-cell type dependent role of type 1 fimbriae genes in the adherence phenotype of super-shedder strains of Escherichia coli O157:H7

Authors: KATANI, ROBAB - Pennsylvania State University; Kudva, Indira; SRINIVASAN, SREENIDHI - Pennsylvania State University; SCHILLING, MEGAN - Pennsylvania State University; COTE, REBECCA - Pennsylvania State University; LI, LINGLING - Pennsylvania State University; DEBROY, CHITRITA - Pennsylvania State University; Arthur, Terrance; KAPUR, VIVEK - Pennsylvania State University; Stasko, Judith

Submitted to: International Journal of Medical Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/3/2021
Publication Date: 5/5/2021
Citation: Katani, R., Kudva, I.T., Srinivasan, S., Schilling, M., Cote, R., Li, L., DebRoy, C., Arthur, T.M., Kapur, V., Stasko, J.A. 2021. Strain and host-cell type dependent role of type 1 fimbriae genes in the adherence phenotype of super-shedder strains of Escherichia coli O157:H7. International Journal of Medical Microbiology. 311(4). https://doi.org/10.1016/j.ijmm.2021.151511.
DOI: https://doi.org/10.1016/j.ijmm.2021.151511

Interpretive Summary: Shiga toxin-producing Escherichia coli O157:H7 (O157) asymptomatically colonize cattle and pose a major threat to human health through consumption of contaminated water and food. Prior studies have suggested that a subset of “super shedder” (SS) cattle excrete O157 several orders of magnitude greater than the majority, and that O157 strains recovered from SS animals exhibit a distinctive strong aggregative pattern of adherence to cells from the bovine rectal anal junction. We here applied a molecular genetic approach to begin to elucidate the mechanisms associated with this striking pattern of adherence. Our results suggest that genes corresponding to the fimbrial operon may play a role in adherence of some SS and a reference strain of O157 to both bovine and human host cells. These findings are noteworthy since previous dogma suggested that the fimbrial operon is genetically “switched off” in O157, and hence was not suspected to play a role in adherence of O157 to host cells. Taken together, the results of our investigations suggest that the adherence phenotype of O157, including SS strains, likely involves complex genetic regulatory pathways of genes corresponding to multiple adherence factors, including those of type 1 fimbriae, in a strain and host cell dependent manner.

Technical Abstract: Shiga toxin-producing Escherichia coli O157:H7 (O157) are zoonotic foodborne pathogens and a significant threat to human health. Asymptomatic cattle harbor the pathogen at the terminal recto-anal junction from where it is shed within the feces. We have previously shown that super-shedder (SS) strains of O157 express a strong, aggregative, non-LEE-dependent adherence phenotype on bovine rectal squamous epithelial (RSE) cells, as well as harbor polymorphisms in non-LEE-dependent adherence related loci. To elucidate the molecular mechanisms contributing to the adherence of SS strains to host cells, we here constructed a series of deletion mutants in type 1 fimbriae in three SS strains (SS17, SS52, SS77) and the well characterized EDL933 strain of O157, and determined their adherence phenotype on bovine RSE and human HEp-2 cells. Consistent with prevailing dogma that fimH expression is genetically switched off in O157, the DeltafimHSS52, DeltafimOPSS52, DeltafimOPSS17, and DeltafimHSS77 strains remained unchanged in adherence phenotype on RSE cells as compared with their wild type counterparts. In striking contrast, the DeltafimHSS17 and DeltafimOPSS77 strains changed from a strong aggregative phenotype in the wild type to a moderate diffuse adherence pattern, while both DeltafimHEDL933 and DeltafimOPEDL933 mutant strains revealed an enhanced binding ability to RSE cells (p less than 0.0001). Further, the analysis also revealed that both DeltafimHSS17 and DeltafimHEDL933 were non-adherent to HEp-2 cells (p less than 0.0001). Complementation of the mutant strains with their respective wild-type genes restored parental phenotypes. Taken together, these results provide compelling evidence for a strain and host-cell type dependent role of fimH and the fim operon in the adherence of O157 to host cells, and suggest that the manifestation of the adherence phenotype of O157 to host cells likely involves a complex coordinately regulated network of genes encoding adherence factors, including those for type 1 fimbriae.