The effect of Campylobacter jejuni challenge on the ileal microbiota and short-chain fatty acids at 28 and 35 days of age

Authors: HAKEEM, WALID GHAZI AL - University Of Georgia; CASON, EMILY - University Of Georgia; VILLANUEVA, KEILA - University Of Georgia; Shanmugasundaram, Revathi; LOURENCO, JEFFERSON - University Of Georgia; SELVARAJ, RAMESH - University Of Georgia

Submitted to: Italian Journal of Animal Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/17/2024
Publication Date: 2/25/2024
Citation: Hakeem, W., Cason, E.E., Villanueva, K.A., Shanmugasundaram, R., Lourenco, J., Selvaraj, R. 2024. The effect of Campylobacter jejuni challenge on the ileal microbiota and short-chain fatty acids at 28 and 35 days of age. Italian Journal of Animal Science. VOL. 23, NO. 1, 299–312. https://doi.org/10.1080/1828051X.2024.2310588.
DOI: https://doi.org/10.1080/1828051X.2024.2310588

Interpretive Summary: In food safety standpoint, Campylobacter jejuni stands as a significant global concern, being the leading foodborne pathogen. Poultry, particularly broilers, serves as the primary reservoir for this bacterium. Broilers typically become infected with C. jejuni through the fecal-oral route at two to three weeks of age and maintain colonization until they reach market age. The gut microbiota plays a pivotal role in providing colonization resistance against pathogens like C. jejuni. This resistance is achieved through mechanisms such as competitive exclusion, bacteriocin production, and the production of short-chain fatty acids (SCFAs). SCFAs are generated by the gut microbiota through the fermentation of complex non-digestible carbohydrates. These SCFAs, in turn, release hydrogen ions (H+) into the chicken gut, reducing pH and bolstering resistance against pathogenic invaders. This study aimed to study the impact of C. jejuni challenge on broiler growth performance, as well as its effects on ileal microbiota, microbial function, and SCFA profiles. The findings revealed that, surprisingly, C. jejuni did not alter the alpha diversity in comparison to the control group. Moreover, it did not significantly affect microbial function or the relative abundances of various microbial taxa, from phyla to species, when compared to the control group. However, a notable observation was a decrease in the ileal concentration of acetate on days 28 and 35, potentially influencing intestinal health. This results highlighted the near-commensal nature of C. jejuni in poultry. However further research needed to explore the impact of C. jejuni on the gut microbiota in broilers at different ages and strains of the pathogen. This knowledge is critical for developing targeted strategies to mitigate the impact of C. jejuni on poultry health and subsequently enhance food safety in the poultry industry.

Technical Abstract: Acetate is a short-chain fatty acid (SCFA) that plays an important role in maintaining intestinal barrier integrity. Campylobacter jejuni (C. jejuni) infection is hypothesised to decrease the presence of acetate-producing bacteria and, consequently, the overall acetate concentration in the ileum, leading to an impaired intestinal barrier. This study aimed to characterize the effect of the C. jejuni challenge on the ileal microbiota and SCFAs concentration in broilers. Sixty broiler chicks were randomly assigned to control and challenge treatments, each with six replications and five birds per replicate. At 21 days of age, birds were inoculated with PBS (control), or 1 108 CFU/bird C. jejuni in the challenge group. Body weight, feed intake and feed conversion ratio were measured weekly. Ileal mucus and contents were collected on days 28 and 35 for microbiome and SCFA analysis. C. jejuni challenge didn’t affect body weight, feed intake and feed conversion ratio at days 28 and 35 compared to the control group. C. jejuni didn’t affect alpha diversity compared to the control group. C. jejuni didn’t alter microbial function nor the relative abundances of the phyla, families, genera and species compared to the control group; however, C. jejuni decreased the ileal concentration of acetate on days 28 (p¼.09) and 35 (p¼.002) compared to the control group. In conclusion, the C. jejuni challenge didn’t alter microbial composition or function and except for the shifts in acetate concentration, it had minimal impact on birds’ intestinal environment, highlighting the near-commensal nature of C. jejuni in broilers.