Avian intestinal mucus modulates Campylobacter jejuni gene expression in a host-specific manner

Authors: Looft, Torey; Cai, Guohong; CHOUDHURY, BISWA - University Of California; Lai, Lisa; Lippolis, John; Reinhardt, Timothy; Sylte, Matthew; CASEY, THOMAS - Retired ARS Employee

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/11/2018
Publication Date: 1/7/2019
Citation: Looft, T.P., Cai, G., Choudhury, B., Lai, L.X., Lippolis, J.D., Reinhardt, T.A., Sylte, M.J., Casey, T.A. 2019. Avian intestinal mucus modulates Campylobacter jejuni gene expression in a host-specific manner. Frontiers in Microbiology. 9:3215. https://doi.org/10.3389/fmicb.2018.03215.
DOI: https://doi.org/10.3389/fmicb.2018.03215

Interpretive Summary: Campylobacter jejuni infection of humans is an important health problem world-wide and is the leading bacterial cause of foodborne illnesses in U.S. The main route for exposure for humans is consumption poultry meat contaminated during processing. C. jejuni is a normal bacteria found in poultry, that lives within the mucus of the intestinal tract, without causing disease in birds. It is not clear why C. jejuni causes disease in some animals and humans, while leaving birds with no symptoms. To understand its activity in birds, we characterized C. jejuni responses to poultry mucus to identify genes turned on in the intestinal tract of birds. We identified genes that are important for survivorship within the poultry gut that were turned on when C. jejuni was exposed to poultry mucus. Our findings are an important step in understanding how C. jejuni responds and interacts in the poultry gut, and may identify ways to reduce C. jejuni in birds.

Technical Abstract: Campylobacter jejuni is a leading cause of bacterial foodborne illness in humans worldwide. However, C. jejuni naturally colonizes poultry without causing pathology where it resides deep within the cecal crypts, colonizing mucus. The presence of mucus may modulate the pathogenicity of C. jejuni in a species-specific manner, where it is pathogenic in humans and asymptomatic in poultry. However, little is known how intestinal mucus from different host species affects C. jejuni gene expression. In this study we characterized the growth and global transcriptome of C. jejuni NCTC11168 cultured in defined media supplemented with host mucus isolated from avian (chicken or turkey) or mammalian (cow, pig, or sheep) sources, or without mucus. C. jejuni showed substantially improved growth over defined media, with mucus from all species, showing that intestinal mucus can be an energy source for C. jejuni. We identified 241 differentially expressed genes from C. jejuni cultured in the presence of mucus after analyzing data across species, compared to defined media alone. Seventy-three of these genes were differentially expressed when C. jejuni was cultured in avian vs. mammalian mucus. Fucose transporter genes were increased regardless of the source of mucus. Genes associated with iron acquisition and resistance to oxidative stress were significantly increased in avian mucus. Surprisingly, many of the differentially expressed genes were flanked by differentially expressed antisense RNA asRNA, suggesting a role in gene regulation. These asRNA may be evidence of pervasive transcription in C. jejuni because they are generated by transcriptional read-through events that cross gene boundaries. This study highlights the interactions between C. jejuni and host mucus and the impact on gene expression, growth and invasion of host cells, suggesting important responses to environmental cues that facilitate intestinal colonization.