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Dietary L-Tryptophan Modulates the Structural and Functional Composition of the Intestinal Microbiome in Weaned Piglets.

ABSTRACT: Background: Intestinal microbiota plays an important role in regulating metabolism, physiology, and immune response of the host. L-Tryptophan (Trp) are metabolized by several genera of bacteria. It remains largely unknown whether Trp can regulate the composition and diversity of the intestinal microbiota and contribute to intestinal homeostasis. Methods: A total of 126 weaning piglets were fed a corn- and soybean meal-based diet supplemented with 0, 0.2, or 0.4% Trp for 4 weeks. The intestinal microbiota was measured by using bacterial 16S rRNA gene-based high-throughput sequencing methods. Metabolites of Trp and short-chain fatty acids (SCFAs) in the hindgut were determined by high-performance liquid chromatography and gas chromatography, respectively. The mRNA levels for aromatic hydrocarbon receptor (AhR), tumor necrotic factor-? (TNF-?), interleukin-8 (IL-8), and protein abundances of tight junction proteins were determined. Results: Compared with the control group, Trp supplementation enhanced piglet growth performance and markedly altered the intestinal microbial composition as evidenced by enhanced alpha and beta diversity in the microbiome (P < 0.05). The abundances of Prevotella, Roseburia, and Succinivibrio genera were enriched, but those of Clostridium sensu stricto and Clostridium XI, opportunistic pathogens, were decreased with dietary Trp supplementation. Analysis of metabolic pathways indicated enhanced indole alkaloid biosynthesis and Trp metabolism, which was validated by elevated concentrations of 3-indoleacetic acid and indole in the intestinal contents of Trp-supplemented piglets (P < 0.05). These changes in Trp metabolites were correlated with activation of AhR and cytochrome p4501 A1 (CYP1A1) in cecum and colonic tissues, and with a decrease in the intestinal mucosal IL-8 mRNA level. Moreover, the protein abundances for zonula occluden (ZO)-1 and occludin were upregulated by Trp supplementation in colonic tissues. Conclusion: Dietary Trp supplementation altered intestinal microbial composition and diversity, improved intestinal mucosal barrier function, activated AhR signaling, and downregulated expression of inflammatory cytokines in the large intestine of weaned piglets. These results indicate a crosstalk between dietary Trp and intestine in nutrition, microbial metabolism, and mucosal immunity.

SUBMITTER: Liang H

PROVIDER: S-EPMC6090026 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Project description:As a microbial tryptophan metabolite, indole-3-carboxaldehyde (ICA) has been suggested to confer benefits to host, such as regulation of intestinal barrier function. This study aimed to elucidate the role of ICA in modulating intestinal homeostasis via using a weaned pig model. Twenty-four weaned piglets were randomly allocated into three groups: the control group (a basal diet), ICA100 group (the basal diet supplemented with 100 mg/kg ICA), and ICA200 group (the basal diet supplemented with 200 mg/kg ICA). The experiment lasted 14 d, and pigs from the control and ICA100 groups were slaughtered. The results showed no significant differences in the average daily gain (ADG) and average daily feed intake (ADFI) among the three groups (P > 0.05). However, the ICA100 group had a lower feed to gain ratio (F:G) (P < 0.05). Dietary ICA supplementation did not alter the villus height, crypt depth, and villus height/crypt depth ratio in the small intestine, and did not change the intestinal permeability and antioxidant parameters (P > 0.05). Intriguingly, ICA treatment significantly increased the jejunal, ileal and colonic indexes in piglets (P < 0.05). Besides, the expression of proliferating cell nuclear antigen (PCNA) in the intestine was up-regulated by ICA treatment. Moreover, in vitro experiments demonstrated that 15 μM ICA significantly accelerated the proliferation activity of IPEC-J2 cells, and increased the expression of the ICA receptor aryl hydrocarbon receptor (AHR) and the proliferation markers PCNA and Cyclin D1 (P < 0.05). In addition, dietary ICA supplementation modulated the intestinal flora, increasing the richness estimators and diversity index, decreasing the abundances of phylum Fibrobacterota and genera Alloprevotella, Prevotella, and Parabacteroides, and enriching the abundance of genera Butyrivibrio. These data reveal a beneficial role for the microbial metabolite ICA on intestinal epithelial proliferation, rather than intestinal barrier function, in weaned piglets.

Project description:Vitamin A (VA) is an important nutrient for weaning piglets. It plays a significant role in the normal formation, development, and maintenance of epithelial cells. Previous studies have shown that VA supplements could improve the host's intestinal barrier function. Therefore, we hypothesized that VA supplements can affect intestinal function in weaned piglets by regulating intestinal stem cells. Thirty-two 21-d-old weaned [(Yorkshire × Landrace) × Duroc] piglets with an average weight of 8.34 ± 0.13 kg were randomly divided into 4 treatment groups, with 1) 2 mg/kg (control), 2) 4 mg/kg, 3) 8 mg/kg, and 4) 16 mg/kg doses of VA, respectively. The experiment lasted for 14 d. Weaned piglets were given ad libitum access to food and water during the test. The ADG (linear, P = 0.020) and G:F (linear, P = 0.005) of the piglets were found to increase significantly from days 8 to 14. The Lgr5+ gene expression (P = 0.012) in the jejunum mucosa of the 16 mg/kg VA group was increased. The jejunum villus height (P = 0.027) and villi surface area (P = 0.035) were significantly increased in the 4 mg/kg VA treatment group. The crypt depth increased significantly in the 4 and 8 mg/kg VA treatment groups (quadratic, P = 0.043), and the ratios of villus height to crypt depth significantly increased in the 16 mg/kg VA group (quadratic, P = 0.015). The maltase (P = 0.032), sucrose (P = 0.041), and alkaline phosphatase activity (linear, P = 0.024) were significantly increased when further supplemented with 4 mg/kg VA. Slc2a2 mRNA abundance was significantly increased in the 2 mg/kg VA group (linear, P = 0.024). Moreover, the budding rates, buddings number per organoid, and Chromogranin A and Muc2 expression of piglet intestinal organoids were significantly reduced (P < 0.05) by VA and its metabolites (retinoic acid). Compared with the control group, the expression of Spp1 and Trop2 increased. These results indicated that VA may increase the stemness of intestinal stem cell in vitro. This study suggested that VA could affect growth performance and intestinal function by regulating intestinal stem cells in the jejunum of weaned piglets.

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Dietary L-Tryptophan Modulates the Structural and Functional Composition of the Intestinal Microbiome in Weaned Piglets.

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