Intestinal location- and age-specific variation of intraepithelial T lymphocytes and mucosal microbiota in pigs

Authors: WIARDA, JAYNE - Oak Ridge Institute For Science And Education (ORISE); WATKINS, HANNAH - Iowa State University; GABLER, NICHOLAS - Iowa State University; Anderson, Christopher; Loving, Crystal

Submitted to: Developmental and Comparative Immunology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/15/2022
Publication Date: 2/1/2023
Citation: Wiarda, J.E., Watkins, H.R., Gabler, N.K., Anderson, C.L., Loving, C.L. 2023. Intestinal location- and age-specific variation of intraepithelial T lymphocytes and mucosal microbiota in pigs. Developmental and Comparative Immunology. 139. Article 104590. https://doi.org/10.1016/j.dci.2022.104590.
DOI: https://doi.org/10.1016/j.dci.2022.104590

Interpretive Summary: Bacterial populations in the intestine can impact overall health, and likely plays a role in immune cell abundance and function in the intestine. Optimal gut health is important for animal production, and understanding shifts in bacteria and immune cells related to age and gut section are important for generation of non-antibiotic products to maximize intestinal health. In the current study, results showed immune cells in the intestinal lining were different across intestinal locations in pigs, but age-specific differences only occurred in specific regions of the intestine. Parallel analysis of intestinal microbes showed differences across intestinal locations and age-specific differences, but again, in a region-specific manner. Collectively, data indicate immune cells in the intestinal lining and respective gut microbes have similar patterns of variation across intestinal locations but have different patterns of variation as pigs age. Noting these patterns is important because understanding different rates of development for immune cells and microbes at different intestinal locations has implications for improving pig intestinal and overall health, particularly through the introduction of products aimed at modulating the microbiota. Pig producers may use this data to consider when intervention strategies may be implemented early in life to impact specific microbial populations and immune cell populations.

Technical Abstract: Intraepithelial T lymphocytes (T-IELs) are T cells located within the intestinal epithelium that provide a first line of immune defense. In pigs, T-IEL abundances and phenotypes are used to infer putative T-IEL functions and vary by intestinal location and age, though investigations regarding porcine T-IELs are relatively limited. Herein, we expand on analyses of porcine intestinal T-IELs to include additional phenotypic designations not previously recognized in pigs. We describe non-conventional CD8alpha+CD8beta- alpha/beta T-IELs that were most prevalent in the distal intestinal tract and primarily CD16+CD27-, a phenotype suggestive of innate-like activation and an activated cell state. Additional T-IEL populations included CD8alpha+CD8beta+ alpha/beta, CD2+CD8alpha+ , and CD2+CD8alpha- gamma/delta T-IELs, with increasing proportions of CD16+CD27- phenotype in the distal intestine. Thus, putative non-conventional, activated T-IELs were most abundant in the distal intestine within multiple gamma/delta and alpha/beta'T-IEL populations. A comparison of T-IEL and respective mucosal microbial community structures across jejunum, ileum, and cecum of 5- and 7-week-old pigs revealed largest community differences were tissue-dependent for both T-IELs and the microbiota. Between 5 and 7 weeks of age, the largest shifts in microbial community compositions occurred in the large intestine, while the largest shifts in T-IEL communities were in the small intestine. Results indicate different rates of community maturation and stabilization for T-IELs and the mucosal microbiota for proximal versus distal intestinal locations between 5 and 7 weeks of age in pigs. Collectively, data emphasize the intestinal tract as a site of location- and age-specific T-IEL and microbial communities that have important implications for understanding intestinal health.