Taeniasis impacts human gut microbiome composition and function

Wenjie Mu, Pingping Ma, Yugui Wang, Yaqi Li, Yingying Ding, Yang Zou, Lixia Pu, Qi Yan, Haoyue Kong, Xiaola Guo, Aijiang Guo, Hailong Li, Shuai Wang
{"title":"Taeniasis impacts human gut microbiome composition and function","authors":"Wenjie Mu, Pingping Ma, Yugui Wang, Yaqi Li, Yingying Ding, Yang Zou, Lixia Pu, Qi Yan, Haoyue Kong, Xiaola Guo, Aijiang Guo, Hailong Li, Shuai Wang","doi":"10.1093/ismejo/wrae213","DOIUrl":null,"url":null,"abstract":"Human taeniasis, caused by Taenia tapeworms, is a global parasitic disease with significant implications for public health and food safety. These tapeworms can grow to considerable sizes and potentially impact the microecology of the host gut. Despite their importance, the effects of Taenia infection on host gut microbiota haven’t been thoroughly investigated. In this study, we conducted a cross-sectional analysis of the gut microbiome in patients infected with Taenia asiatica (n = 87) compared to healthy controls (n = 79) in the Dali cohort, China. We also performed a longitudinal assessment of microbial changes following deworming in a subset of patients (n = 24). Our findings reveal a significant shift in gut microbial composition, characterized by increased alpha-diversity and an enrichment of Prevotella-driven enterotypes in infected patients compared to healthy controls. The stability of these microbial features post-deworming varied widely among individuals and was lower in those with lower initial alpha diversity and Prevotella-enterotype before deworming. We observed a significant depletion of Bifidobacterium species in infected individuals, regardless of enterotypes, and these prebiotics did not recover post-deworming. Metabolic network analysis and in vitro experiments suggest that the reduction of Bifidobacterium was linked to metabolic competition for ecological niches or nutrients, particularly stachyose, from other microbes rather than the parasitism itself. Furthermore, our machine learning analysis demonstrated that taxa associated with Bifidobacterium in stachyose metabolism could robustly predict infection but could not predict deworming. This study highlights the substantial impact of taeniasis on the human gut microbiome and overall gut health.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"235 1","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"The ISME Journal","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/ismejo/wrae213","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0

Abstract

Human taeniasis, caused by Taenia tapeworms, is a global parasitic disease with significant implications for public health and food safety. These tapeworms can grow to considerable sizes and potentially impact the microecology of the host gut. Despite their importance, the effects of Taenia infection on host gut microbiota haven’t been thoroughly investigated. In this study, we conducted a cross-sectional analysis of the gut microbiome in patients infected with Taenia asiatica (n = 87) compared to healthy controls (n = 79) in the Dali cohort, China. We also performed a longitudinal assessment of microbial changes following deworming in a subset of patients (n = 24). Our findings reveal a significant shift in gut microbial composition, characterized by increased alpha-diversity and an enrichment of Prevotella-driven enterotypes in infected patients compared to healthy controls. The stability of these microbial features post-deworming varied widely among individuals and was lower in those with lower initial alpha diversity and Prevotella-enterotype before deworming. We observed a significant depletion of Bifidobacterium species in infected individuals, regardless of enterotypes, and these prebiotics did not recover post-deworming. Metabolic network analysis and in vitro experiments suggest that the reduction of Bifidobacterium was linked to metabolic competition for ecological niches or nutrients, particularly stachyose, from other microbes rather than the parasitism itself. Furthermore, our machine learning analysis demonstrated that taxa associated with Bifidobacterium in stachyose metabolism could robustly predict infection but could not predict deworming. This study highlights the substantial impact of taeniasis on the human gut microbiome and overall gut health.
泰纳丝虫病影响人类肠道微生物组的组成和功能
由太安绦虫引起的人类太安虫病是一种全球性寄生虫病,对公共卫生和食品安全有重大影响。这些绦虫可以长到相当大的尺寸,并可能影响宿主肠道的微生态。尽管它们很重要,但人们还没有深入研究过疟原虫感染对宿主肠道微生物群的影响。在这项研究中,我们对中国大理队列中感染亚洲洮蛲的患者(87 人)与健康对照组(79 人)的肠道微生物组进行了横断面分析。我们还对一部分患者(24 人)驱虫后的微生物变化进行了纵向评估。我们的研究结果表明,与健康对照组相比,感染患者的肠道微生物组成发生了重大变化,其特点是α-多样性增加,前驱菌驱动的肠型富集。驱虫后这些微生物特征的稳定性在个体间差异很大,在驱虫前初始α-多样性和普雷沃氏菌肠型较低的个体中,其稳定性更低。我们观察到,无论肠道型如何,感染者体内的双歧杆菌都会大量减少,而这些益生菌在驱虫后并没有恢复。代谢网络分析和体外实验表明,双歧杆菌的减少与其他微生物对生态位或营养物质(尤其是水苏糖)的代谢竞争有关,而非寄生本身。此外,我们的机器学习分析表明,在水苏糖代谢过程中与双歧杆菌相关的类群可以稳健地预测感染情况,但不能预测驱虫情况。这项研究强调了泰尼丝虫病对人类肠道微生物组和整体肠道健康的重大影响。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
自引率
0.00%
发文量
0
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信