Cecal microbial hydrogen cycling potential is linked to agriculturally desirable phenotypes in chickens

Authors: RAMIREZ, GUSTAVO - Western University Of Health Sciences; KESHRI, JITENDRA - Western University Of Health Sciences; VAHRSON, ISABELLA - Western University Of Health Sciences; GARBER, ARKAIDY - Arizona State University; Berrang, Mark; Cox Jr, Nelson; SEAL, BRUCE - Oregon State University; SAMUEL, AGGREY - University Of Georgia; OAKLEY, BRIAN - Western University Of Health Sciences

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/19/2022
Publication Date: 6/21/2022
Citation: Ramirez, G., Keshri, J., Vahrson, I., Garber, A., Berrang, M.E., Cox Jr, N.A., Seal, B., Samuel, A., Oakley, B. 2022. Cecal microbial hydrogen cycling potential is linked to agriculturally desirable phenotypes in chickens. Frontiers in Microbiology. https://doi.org/10.3389/fvets.2022.904698.
DOI: https://doi.org/10.3389/fvets.2022.904698

Interpretive Summary: The gut microbiome of broiler chickens includes all bacteria living or growing within the intestines. These bacteria are important to the growing bird as an ideal balance of gut bacteria helps assure proper digestion and utilization of feed. We have shown that broiler chicks that are treated with a transplant of gut bacteria from fast growing adult broilers have better agricultural performance characteristics (feed conversion and weight gain) than those that do not receive the transplant. It is not understood how exactly gut bacteria work to improve performance of growing birds. Herein, we used metagenomic techniques to examine the gut microbiome of broiler chickens that had received a performance enhancing transplant in an effort to better understand the mechanism of improved growth. We found that the microbes present in the intestines of treated birds had more genetic potential to remove hydrogen gas which is a natural product of feed digestion. Our data suggest that the improved removal of hydrogen results in a more efficient fermentation process and may explain some of the performance advantage noted in broiler that receive gut microbiome transplant early in life.

Technical Abstract: In chickens, early life exposure to environmental microbes has long-lasting impacts on gastrointestinal microbiome development and, ultimately, via uncharacterized mechanisms involving host-microbiome interactions, life-long growth- and health-related performance. In this study, we show that administrating a fecal microbiome transplant to newly hatched chicks results in significantly higher body mass of birds at market age. To assess the potential mechanisms through which early life microbiome transplants affect adult bird phenotype, we used a top-down comparative genomic, metagenomic, and gene-targeted approach. Early life microbial exposure had a significant and exclusive effect on cecal microbial composition and activities as opposed to other gastrointestinal tract segments. Within the ceca of six-week-old birds that received an early life microbiome transplant, microbial lineages with the potential to serve as hydrogen sinks were most differentially enriched. Interestingly, microbiome transplantation did not affect composition and predicted function of cecal fermenters. Together, our results suggests that thermodynamic regulation, via the promotion of a few lineages serving as cecal hydrogen sinks as opposed to large-scale community structuring, may enhance cecal fermentative efficiency and dietary energy harvest capacity. We thereby provide the first mechanism of action through which early-life microbiome transplants modulate market-relevant phenotypes in poultry and expand the current frontiers for sustainable agriculture.