Recent advances in the application of microbiota transplantation in chickens

Abstract

Extensive evidence demonstrates that a healthy and well-balanced gut microbiota profoundly influences host nutrient absorption, immunity, and metabolism. Unlike mammals, early microbiota colonization in commercial poultry largely depends on the environment as chicks hatch in incubators under a relatively sterile environment (egg and incubator sterilization) without maternal-offspring interaction. The early gut microbiota remains unsaturated, providing a critical window for modulation and influencing the subsequent microbiota succession, which may have long-term health outcomes. Microbiota transplantation (MT) involves transferring the microbiota from a donor to a recipient to modulate the recipient's microbiota toward a desired state. Successfully applied in human medicine, MT is also gaining attention in poultry production to modulate intestinal health. This review comprehensively explores factors affecting MT, its mechanisms, and its potential applications in chickens, providing insights for further research and commercial use.

Keywords: Behavior; Gut health; Immunity; Metabolism; Microbiota colonization; Microbiota composition; Microbiota modulation.

Fig. 1

Overview of microbiota sources, processing steps, and delivery methods of microbiota transplantation (MT). Microbiota sources for MT include feces, intestinal content, fermentation products, and used litter. Feces and intestinal content are typically diluted with a buffer (e.g., saline or phosphate-buffered saline), homogenized, and filtered to remove large particles, after which they are ready for use. Fermentation products are generated by culturing healthy donor microbiota in nutrient-rich bioreactors for several days, resulting in a ready-to-use product. Delivery methods vary, with gavage being the most common approach. The prepared inoculum can also be sprayed onto eggs, feed, wood shavings, or directly onto chicks. Additionally, microbiota can be delivered through water. Reusing litter directly is also suggested, as it contains mature and abundant microbiota. Figure created in https://BioRender.com

Fig. 2

Effects of microbiota transplantation (MT) on performance, behavior, gut function, immune function, and metabolism of recipient chickens. Performance: MT enhances feed intake and body weight, reducing the feed conversion ratio (FCR). It improves ovarian function by modulating antiapoptotic and proapoptotic gene expression, hence increasing egg production. Behavior: MT influences behavior via the gut-brain axis. Microbiota-derived metabolites (e.g., p-cresol sulfate, indole-3-acetic acid) can enter the peripheral vascular system and disrupt the blood–brain barrier, facilitating cytokines to enter the brain. Serotonin (5-HT), which originates from enterochromaffin cells or luminal tryptophan, plays a key role in behavior. Additionally, the microbiota regulates behavior through endocrine signals, neurotransmitters, N-glycan, and glutamate metabolism. MT reduces feather pecking, fearfulness, and aggression while promoting active responses. Gut Function: MT-derived microbiota produce short-chain fatty acids (SCFAs), enzymes, cofactors, and vitamins, enhancing carbohydrate and amino acid metabolism, as well as secondary metabolite biosynthesis. MT improves villus height, reduces crypt depth, and increases the villus-to-crypt (V/C) ratio. It also upregulates the expression of Mucin 2 (MUC2), MUC13, Zonula occludens 1 (ZO1), and Claudin 1 (CLDN1), strengthening gut integrity. Immune Function: MT enhances gut immunity by increasing secretory IgA (sIgA), mucins, and antimicrobial peptides. Microbiota activate toll-like receptors (TLRs) via TRIF and MyD88 pathways, promoting cytokine production. MT also supports the development of the thymus and bursa of Fabricius, which are critical for T and B cell maturation, and increases dendritic cells (DCs). Additionally, MT modulates immune function through the gut-lung and gut-liver axes. Metabolism: MT improves phosphorus absorption by regulating intestinal phosphate transporters and creating an acidic gut environment via SCFAs, and also increases tibia length. MT regulates fat metabolism by modulating fat synthesis and fat breakdown genes in the liver and abdominal fat. Red upward arrows indicate promotion, while blue downward arrows indicate inhibition. Figure created in https://BioRender.com