Xylanase enhances gut microbiota-derived butyrate to exert immune-protective effects in a histone deacetylase-dependent manner.

IF 13.8 1区生物学 Q1 MICROBIOLOGY

Microbiome Pub Date : 2024-10-21 DOI:10.1186/s40168-024-01934-6

Tong Wang, Nannan Zhou, Feifei Ding, Zhenzhen Hao, Jorge Galindo-Villegas, Zhenyu Du, Xiaoyun Su, Meiling Zhang

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引用次数: 0

Abstract

Background: Commensal bacteria in the intestine release enzymes to degrade and ferment dietary components, producing beneficial metabolites. However, the regulatory effects of microbial-derived enzymes on the intestinal microbiota composition and the influence on host health remain elusive. Xylanase can degrade xylan into oligosaccharides, showing wide application in feed industry.

Results: To validate the immune-protective effects of xylanase, Nile tilapia was used as the model and fed with xylanase. The results showed that dietary xylanase improved the survival rate of Nile tilapia when they were challenged with Aeromonas hydrophila. The transcriptome analysis showed significant enrichment of genes related to interleukin-17d (il-17d) signaling pathway in the xylanase treatment group. High-throughput sequencing revealed that dietary xylanase altered the composition of the intestinal microbiota and directly promoted the proliferation of Allobaculum stercoricanis which could produce butyrate in vitro. Consequently, dietary xylanase supplementation increased the butyrate level in fish gut. Further experiment verified that butyrate supplementation enhanced the expression of il-17d and regenerating islet-derived 3 gamma (reg3g) in the gut. The knockdown experiment of il-17d confirmed that il-17d is necessary for butyrate to protect Nile tilapia from pathogen resistance. Flow cytometry analysis indicated that butyrate increased the abundance of IL-17D⁺ intestinal epithelial cells in fish. Mechanistically, butyrate functions as an HDAC3 inhibitor, enhancing il-17d expression and playing a crucial role in pathogen resistance.

Conclusion: Dietary xylanase significantly altered the composition of intestinal microbiota and increased the content of butyrate in the intestine. Butyrate activated the transcription of il-17d in intestinal epithelial cells by inhibiting histone deacetylase 3, thereby protecting the Nile tilapia from pathogen infection. This study elucidated how microbial-derived xylanase regulates host immune function, providing a theoretical basis for the development and application of functional enzymes. Video Abstract.

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木聚糖酶以组蛋白去乙酰化酶依赖的方式增强肠道微生物群衍生的丁酸盐，从而发挥免疫保护作用。

背景：肠道中的共生细菌会释放酶来降解和发酵食物成分，产生有益的代谢物。然而，微生物衍生酶对肠道微生物群组成的调控作用以及对宿主健康的影响仍然难以捉摸。木聚糖酶可将木聚糖降解为低聚糖，在饲料行业有广泛应用：结果：为了验证木聚糖酶的免疫保护作用，以尼罗罗非鱼为模型，用木聚糖酶饲喂。结果表明，当尼罗罗非鱼受到嗜水气单胞菌挑战时，日粮中的木聚糖酶可提高其存活率。转录组分析表明，在木聚糖酶处理组中，与白细胞介素-17d（il-17d）信号通路相关的基因显著富集。高通量测序显示，膳食木聚糖酶改变了肠道微生物群的组成，并直接促进了可在体外产生丁酸的Allobaculum stercoricanis的增殖。因此，膳食中添加木聚糖酶可提高鱼类肠道中的丁酸盐含量。进一步的实验证实，补充丁酸盐可提高肠道中 il-17d 和再生胰岛衍生 3 γ（reg3g）的表达。il-17d的敲除实验证实，il-17d是丁酸盐保护尼罗罗非鱼抵抗病原体的必要条件。流式细胞术分析表明，丁酸盐增加了鱼体内IL-17D+肠上皮细胞的丰度。从机理上讲，丁酸盐是一种 HDAC3 抑制剂，可提高 IL-17d 的表达，在抗病原体中发挥重要作用：结论：膳食木聚糖酶显著改变了肠道微生物群的组成，增加了肠道中丁酸盐的含量。丁酸盐通过抑制组蛋白去乙酰化酶 3 激活肠上皮细胞中 il-17d 的转录，从而保护尼罗罗非鱼免受病原体感染。这项研究阐明了微生物衍生的木聚糖酶如何调节宿主免疫功能，为功能酶的开发和应用提供了理论依据。视频摘要。

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来源期刊

Microbiome MICROBIOLOGY-

CiteScore

21.90

自引率

2.60%

发文量

198

审稿时长

4 weeks

期刊介绍： Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.