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Mining chicken ileal microbiota for immunomodulatory microorganisms

The ISME Journal volume 17, pages 758–774 (2023)Cite this article

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Abstract

The gut microbiota makes important contributions to host immune system development and resistance to pathogen infections, especially during early life. However, studies addressing the immunomodulatory functions of gut microbial individuals or populations are limited. In this study, we explore the systemic impact of the ileal microbiota on immune cell development and function of chickens and identify the members of the microbiota involved in immune system modulation. We initially used a time-series design with six time points to prove that ileal microbiota at different succession stages is intimately connected to immune cell maturation. Antibiotics perturbed the microbiota succession and negatively affected immune development, whereas early exposure to the ileal commensal microbiota from more mature birds promoted immune cell development and facilitated pathogen elimination after Salmonella Typhimurium infection, illustrating that early colonization of gut microbiota is an important driver of immune development. Five bacterial strains, Blautia coccoides, Bacteroides xylanisolvens, Fournierella sp002159185, Romboutsia lituseburensis, and Megamonas funiformis, which are closely related to the immune system development of broiler chickens, were then screened out and validated for their immunomodulatory properties. Our results provide insight into poultry immune system–microbiota interactions and also establish a foundation for targeted immunological interventions aiming to combat infectious diseases and promote poultry health and production.

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Fig. 1: Overview of experiment design.
Fig. 2: Temporal and spatial development of ileum microbiota in broiler chickens.
Fig. 3: Sequential waves of immune cell expansion after birth.
Fig. 4: Interaction between bacteria and the proportion of immune cells.
Fig. 5: The antibiotic chlortetracycline interferes with the development of ileum microbiota and immune cells.
Fig. 6: Early exposure to ileal commensal microbiota from more mature individuals influences the immune cell composition of chickens.
Fig. 7: Microbiota transplantation enhances the resistance to Salmonella Typhimurium infection of broiler chickens.
Fig. 8: Immunomodulatory properties of five bacterial strains.

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Data availability

The raw 16S rRNA gene sequencing data of luminal microbiota from the antibiotic-untreated broiler chickens were obtained from NCBI BioProject PRJNA817429 (unpublished data from our own laboratory), and additional raw 16S rRNA gene sequencing data have been deposited in NCBI BioProject PRJNA904673. The genome data have been deposited in NCBI BioProject PRJNA903494 and PRJNA902159. The transcriptome data have been deposited in NCBI BioProject PRJNA904665. Raw datasets used for multicolor flow cytometry and qRT-PCR are available on FigShare (https://doi.org/10.6084/m9.figshare.21825042).

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (32172685), the National Key Research and Development Program of China (2022YFD1300400) and the 2115 Talent Development Program of China Agricultural University. Figure 1 was produced with BioRender.

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Authors and Affiliations

  1. State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, 100193, Beijing, China

    Yan Liu, Yuqing Feng, Xinyue Yang, Zhengtian Lv, Peng Li, Meihong Zhang, Fuxiao Wei, Xiaolu Jin, Yongfei Hu, Yuming Guo & Dan Liu

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Contributions

DL designed the project. YL carried out the experimental work and drafted the manuscript. MZ carried out bioinformatic analyses. YF, XY, ZL, PL and FW collected samples. All the other authors revised and edited the manuscript. All authors read and approved the final manuscript.

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Correspondence to Dan Liu.

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All the experiments were reviewed and approved by China Agricultural University Animal Care and Use Committee (statement no. AW30112202-1-1).

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Liu, Y., Feng, Y., Yang, X. et al. Mining chicken ileal microbiota for immunomodulatory microorganisms. ISME J 17, 758–774 (2023). https://doi.org/10.1038/s41396-023-01387-z

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