Faecalibacterium prausnitzii-derived outer membrane vesicles reprogram gut microbiota metabolism to alleviate Porcine Epidemic Diarrhea Virus infection.

IF 13.8 1区生物学 Q1 MICROBIOLOGY

Microbiome Pub Date : 2025-04-02 DOI:10.1186/s40168-025-02078-x

JunHong Xing, TianMing Niu, Tong Yu, BoShi Zou, ChunWei Shi, YingJie Wang, ShuHui Fan, MingHan Li, MeiYing Bao, Yu Sun, KuiPeng Gao, JingJing Qiu, DongXing Zhang, Nan Wang, YanLong Jiang, HaiBin Huang, Xin Cao, Yan Zeng, JianZhong Wang, ShuMin Zhang, JingTao Hu, Di Zhang, WuSheng Sun, GuiLian Yang, WenTao Yang, ChunFeng Wang

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Abstract

Background: The Porcine Epidemic Diarrhea Virus (PEDV) is one of the major challenges facing the global pig farming industry, and vaccines and treatments have proven difficult in controlling its spread. Faecalibacterium prausnitzii (F.prausnitzii), a key commensal bacterium in the gut, has been recognized as a promising candidate for next-generation probiotics due to its potential wide-ranging health benefits. A decrease in F.prausnitzii abundance has been associated with certain viral infections, suggesting its potential application in preventing intestinal viral infections. In this study, we utilized a piglet model to examine the potential role of F.prausnitzii in PEDV infections.

Results: A piglet model of PEDV infection was established and supplemented with F.prausnitzii, revealing that F.prausnitzii mitigated PEDV infection. Further studies found that outer membrane vesicles (OMVs) are the main functional components of F.prausnitzii, and proteomics, untargeted metabolomics, and small RNA-seq were used to analyze the composition of OMVs. Exhaustion of the gut microbiota demonstrated that the function of Fp. OMVs relies on the presence of the gut microbiota. Additionally, metagenomic analysis indicated that Fp. OMVs altered the gut microbiota composition, enhancing the abundance of Faecalibacterium prausnitzii, Prevotellamassilia timonensis, and Limosilactobacillus reuteri. Untargeted metabolomics analysis showed that Fp. OMVs increased phosphatidylcholine (PC) levels, with PC identified as a key metabolite in alleviating PEDV infection. Single-cell sequencing revealed that PC altered the relative abundance of intestinal cells, increased the number of intestinal epithelial cells, and reduced necroptosis in target cells. PC treatment in infected IPEC-J2 and Vero cells alleviated necroptosis and reduced the activation of the RIPK1-RIPK3-MLKL signaling axis, thereby improving PEDV infection.

Conclusion: F.prausnitzii and its OMVs play a critical role in mitigating PEDV infections. These findings provide a promising strategy to ameliorate PEDV infection in piglets. Video Abstract.

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普氏粪杆菌衍生的外膜囊泡可重塑肠道微生物群代谢，从而缓解猪流行性腹泻病毒感染。

背景：猪流行性腹泻病毒（PEDV）是全球养猪业面临的主要挑战之一，疫苗和治疗已被证明难以控制其传播。prausnitzii粪杆菌（Faecalibacterium prausnitzii）是肠道中一种重要的共生菌，由于其潜在的广泛健康益处，已被认为是下一代益生菌的有希望的候选菌。prausnitzii丰度的减少与某些病毒感染有关，提示其在预防肠道病毒感染方面的潜在应用。在这项研究中，我们利用仔猪模型来研究普氏f.p auusnitzii在PEDV感染中的潜在作用。结果：建立了猪PEDV感染仔猪模型，并添加了f .prausnitzi，显示f .prausnitzi能减轻PEDV感染。进一步研究发现，外膜囊泡（omv）是F.prausnitzii的主要功能成分，并利用蛋白质组学、非靶向代谢组学和小RNA-seq分析了omv的组成。肠道菌群的衰竭证明了Fp的功能。omv依赖于肠道微生物群的存在。此外，宏基因组分析表明Fp。omv改变了肠道菌群组成，增加了prausnitzii Faecalibacterium， timonensis Prevotellamassilia和reuteri Limosilactobacillus。非靶向代谢组学分析显示，Fp。omv增加了磷脂酰胆碱（PC）水平，PC被认为是缓解PEDV感染的关键代谢物。单细胞测序显示，PC改变了肠细胞的相对丰度，增加了肠上皮细胞的数量，减少了靶细胞的坏死。PC治疗感染的IPEC-J2和Vero细胞可减轻坏死坏死，降低RIPK1-RIPK3-MLKL信号轴的激活，从而改善PEDV感染。结论：prausnitzi及其omv在缓解PEDV感染中起关键作用。这些发现为改善仔猪PEDV感染提供了一种有希望的策略。视频摘要。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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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.