Oral Treatment With Ileal Spores Triggers Immunometabolic Shifts in Chicken Gut

Abstract

The animal gut is a major site affecting productivity via its role in mediating functions like food conversion and pathogen colonization. Live microorganisms like probiotics are widely used to improve poultry productivity. However, given that chicks receive their microbiota from the environment at-hatch, a bacterial treatment that can stimulate gut immune maturation in early life can benefit animal health. Thus, our lab has begun investigating alternative means to improve poultry health via single inoculation with microbial spores. In this study, we orally-inoculated day-old chicks with ileal scrapings (ISs) enriched for spores via chloroform treatment (SPORE) or non-treated (CON). At 3, 7, and 14 days post-inoculation (dpi), gut permeability was measured via FITC-dextran assay in serum. Additionally, small intestinal scrapings (SISs) were tested for in vitro Salmonella killing and total IgA. Lastly, distal ileum was either fixed or flash-frozen for microscopy or kinome peptide array, respectively. Using bacterial 16S rRNA gene sequencing, SPORE and CON inocula were highly-similar in bacterial composition. However, spores were detected in SPORE but not in CON inoculum. Segmented filamentous bacteria (SFB) filaments were observed in the distal ileum in SPORE birds as early as 3 dpi and all birds at 7 and 14 dpi. Additionally, SFB were detected via PCR in the ceca, colonizing all SPORE birds at 3 dpi. At 3 dpi, SPORE birds exhibited lower gut permeability vs. CON. In SPORE birds, SISs induced greater Salmonella growth in vitro at 3 dpi yet significantly-reduced Salmonella load at 7 and 14 dpi compared to CON in an IgA-independent manner. SPORE distal ileal tissue exhibited unique upregulation of several immunometabolic processes vs. CON birds, including innate (Toll-like receptor, JAK-STAT) and adaptive (T/B cell receptor, T H 17 differentiation) immune pathways, PI3K/Akt signaling, mTOR signaling, and insulin-related pathways. Collectively, these data suggest oral inoculation with ileal spores generally-improved gut health. Importance: We report that ileal, spore-forming commensal microbes have potent effects on ileum immunometabolism. Additionally, we identify a functional ileal phenotype in spore-treated chickens, which matched several of the observed immunometabolic changes and was associated with SFB colonization in the ileum.

Ileal Microbiota Alters the Immunity Statues to Affect Body Weight in Muscovy Ducks

“…Alternatively, early colonization of probiotics (17,18) and fecal microbiota transplantation (19) can accelerate the maturation of the intestinal microbes and improve the growth performance of the host. To date, most investigations on the ileal microbiota in poultry is about chickens (20)(21)(22)(23). However, little is known about the bacteria in the ileum of Muscovy ducks.…”

Are there consistent effects of gut microbiota composition on performance, productivity and condition in poultry?

“…Due to their reduced genomes, SFBs are highly dependent on their hosts for many metabolic functions and consequently hard to culture ( Danzeisen et al, 2013 ). They can be efficiently administrated as spores ( Redweik et al, 2020 ). Meinen-Jochum et al (2023) showed that SFB treatment in chicken can suppress Salmonella infection and cause a significant decrease in total Enterobacteriaceae.…”

Poultry gut health and beyond

“…Candidatus Savagella is segmented and filamentous in shape and attaches to the epithelium of the ileum. These organisms are also present in the chicken ileum ( Redweik et al., 2020 ).…”