Fecal microbiota transplantation reduces Campylobacter jejuni colonization in young broiler chickens challenged by oral gavage but not by seeder birds

Authors: PANG, JINJI - Iowa State University; BEYI, ASHENAFI FEYISA - Iowa State University; Looft, Torey; ZHANG, QIJING - Iowa State University; SAHIN, ORHAN - Iowa State University

Submitted to: Antibiotics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/30/2023
Publication Date: 10/2/2023
Citation: Pang, J., Beyi, A., Looft, T.P., Zhang, Q., Sahin, O. 2023. Fecal microbiota transplantation reduces Campylobacter jejuni colonization in young broiler chickens challenged by oral gavage but not by seeder birds. Antibiotics. 12(10). Article 1503. https://doi.org/10.3390/antibiotics12101503.
DOI: https://doi.org/10.3390/antibiotics12101503

Interpretive Summary: Campylobacter is a major food safety concern and is transmitted to humans via contaminated poultry products. Limiting Campylobacter levels in the poultry intestine may reduce the risk of product contamination. There are differences in the gut bacteria on farms that consistently produce Campylobacter-negative chicken flocks to flocks consistently Campylobacter-positive. To further determine if gut bacteria might influence Campylobacter status, we conducted two animal trials where newly hatched chickens were given intestinal contents from mature Campylobacter-free chickens (fecal microbiota transplantation (FMT)) to evaluate the effect on subsequent Campylobacter colonization. First, FMT significantly impacted the gut bacterial composition of birds. Additionally, FMT limited cecal Campylobacter colonization in birds that were directly inoculated with Campylobacter, but not when Campylobacter was introduced by co-mingling infected birds with uninfected birds. These findings indicate that even though FMT can impact the development of the gut microbiota in young chickens, its inhibitory effect on Campylobacter colonization varies and is potentially influenced by the route of Campylobacter exposure. The development of novel Campylobacter control strategies like FMT, is essential to improve poultry food safety, and has the potentially to reduce human foodborne illness.

Technical Abstract: Campylobacter spp., particularly C. jejuni and C. coli, are major food safety concerns, transmitted to humans mainly via contaminated poultry meat. In a previous study, we found that some com-mercial broiler farms consistently produced Campylobacter-negative flocks while others consist-ently reared Campylobacter-positive flocks, and significant differences in the gut microbiota com-positions between the two types of farm categories were revealed. Therefore, we hypothesized that gut microbiota influences Campylobacter colonization in poultry and that the microbiota from Campylobacter-negative flocks may confer colonization resistance to Campylobacter in the chicken intestine. In this study, two fecal microbiota transplantation (FMT) trials were performed to ex-amine the hypothesis. Newly hatched chicks were given FMT via oral gavage of the cecal content of Campylobacter-free adult chickens (treatment groups) or PBS (control groups) before the feed consumption. Approximately two weeks after the FMT, the birds were challenged with C. jejuni either by oral gavage (trial 1) or by co-mingling with Campylobacter-colonized seeder birds (trial 2) to evaluate the potential protective effect of FMT. Cecal contents were collected periodically to determine Campylobacter colonization levels via culture and microbiota compositions via 16S rRNA gene sequencing. FMT reduced cecal Campylobacter colonization significantly in trial 1, but not in trial 2 although FMT significantly impacted the diversity and compositions of the gut mi-crobiota in both trials. Several genera, such as Butyricimonas, Parabacteroides, Parasutterella, Bi-lophila, Fournierella, Phascolarctobacterium, and Helicobacter had increased abundance in the FMT-treated groups in both trials. Furthermore, Campylobacter abundance was found to be nega-tively correlated with Escherichia and Ruminococcus_torques_group genera. These findings indi-cate that even though FMT with adult cecal microbiota can positively affect the subsequent de-velopment of the gut microbiota in young broilers, its inhibitory effect on Campylobacter coloniza-tion varies and appear to be influenced by the challenge models.