Phenotypic, genotypic and proteomic variations between poor and robust colonizing Campylobacter jejuni strains.

Authors: SUNG, KIDON - Us Food & Drug Administration (FDA); GAO, YUAN - Us Food & Drug Administration (FDA); YU, LI-RONG - Us Food & Drug Administration (FDA); CHON, JUNGWHAN - Inje University; HIETT, KELLI - Us Food & Drug Administration (FDA); LINE, ERIC - Retired ARS Employee; KWEON, OHGEW - Us Food & Drug Administration (FDA); PARK, MISEON - Us Food & Drug Administration (FDA); KHAN, SAEED - Us Food & Drug Administration (FDA)

Submitted to: Microbial Pathogenesis
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/26/2024
Publication Date: 6/27/2024
Citation: Sung, K., Gao, Y., Yu, L., Chon, J., Hiett, K.L., Line, E.J., Kweon, O., Park, M., Khan, S.A. 2024. Phenotypic, genotypic and proteomic variations between poor and robust colonizing Campylobacter jejuni strains.. Microbial Pathogenesis. 193: 102766. https://doi.org/10.1016/j.micpath.2024.106766.
DOI: https://doi.org/10.1016/j.micpath.2024.106766

Interpretive Summary: Campylobacter jejuni is one of the major causes of bacterial gastrointestinal disease in humans worldwide. This foodborne pathogen colonizes the intestinal tracts of chickens, and consumption of chicken and poultry products is identified as a common route of transmission. Two C. jejuni strains were analyzed after oral challenge with C. jejuni per chick; one strain was a robust colonizer (A74/C) and the other a poor colonizer (A74/O). Strains A74/C and A74/O were genotypically similar; however, extensive phenotypic differences in growth rate, biofilm production, and in vitro adherence, invasion, intracellular survival, and transcytosis were found. Additional analyses showed that carbon metabolism and motility proteins were distinctively overexpressed in strain A74/C. The robust colonizer also exhibited significantly increased expression of proteins linked to adhesion, invasion, chemotaxis, energy, protein synthesis, heat shock proteins, iron regulation, two-component regulatory systems, and multidrug efflux pump. These findings demonstrate that chick colonization of C. jejuni is not a simple process involving just a few colonization factors, but one incorporating many colonization factors, which together may contribute to commensalism in the chicken.

Technical Abstract: Campylobacter jejuni is one of the major causes of bacterial gastrointestinal disease in humans worldwide. This foodborne pathogen colonizes the intestinal tracts of chickens, and consumption of chicken and poultry products is identified as a common route of transmission. We analyzed two C. jejuni strains after oral challenge with 10 (5) CFU/ml of C. jejuni per chick; one strain was a robust colonizer (A74/C) and the other a poor colonizer (A74/O). We also found extensive phenotypic differences in growth rate, biofilm production, and in vitro adherence, invasion, intracellular survival, and transcytosis. Strains A74/C and A74/O were genotypically similar with respect to their whole genome alignment, core genome, and ribosomal MLST, MLST, flaA, porA, and PFGE typing. The global proteomes of the two congenic strains were quantitatively analyzed by ultra-high performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS) and 618 and 453 proteins were identified from A74/C and A74/O isolates, respectively. Cluster of Orthologous Groups (COG) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses showed that carbon metabolism and motility proteins were distinctively overexpressed in strain A74/C. The robust colonizer also exhibited a unique proteome profile characterized by significantly increased expression of proteins linked to adhesion, invasion, chemotaxis, energy, protein synthesis, heat shock proteins, iron regulation, two-component regulatory systems, and multidrug efflux pump. Our study underlines phenotypic, genotypic, and proteomic variations of the poor and robust colonizing C. jejuni strains, suggesting that several factors may contribute to mediating the different colonization potentials of the isogenic isolates.