Dietary fiber monosaccharide content alters gut microbiome composition and fermentation.

IF 3.9 2区 生物学 Q2 BIOTECHNOLOGY & APPLIED MICROBIOLOGY
Applied and Environmental Microbiology Pub Date : 2024-08-21 Epub Date: 2024-07-15 DOI:10.1128/aem.00964-24
Nick Jensen, Maria Maldonado-Gomez, Nithya Krishnakumar, Cheng-Yu Weng, Juan Castillo, Dale Razi, Karen Kalanetra, J Bruce German, Carlito B Lebrilla, David A Mills, Diana H Taft
{"title":"Dietary fiber monosaccharide content alters gut microbiome composition and fermentation.","authors":"Nick Jensen, Maria Maldonado-Gomez, Nithya Krishnakumar, Cheng-Yu Weng, Juan Castillo, Dale Razi, Karen Kalanetra, J Bruce German, Carlito B Lebrilla, David A Mills, Diana H Taft","doi":"10.1128/aem.00964-24","DOIUrl":null,"url":null,"abstract":"<p><p>Members of the mammalian gut microbiota metabolize diverse complex carbohydrates that are not digested by the host, which are collectively labeled \"dietary fiber.\" While the enzymes and transporters that each strain uses to establish a nutrient niche in the gut are often exquisitely specific, the relationship between carbohydrate structure and microbial ecology is imperfectly understood. The present study takes advantage of recent advances in complex carbohydrate structure determination to test the effects of fiber monosaccharide composition on microbial fermentation. Fifty-five fibers with varied monosaccharide composition were fermented by a pooled feline fecal inoculum in a modified MiniBioReactor array system over a period of 72 hours. The content of the monosaccharides glucose and xylose was significantly associated with the reduction of pH during fermentation, which was also predictable from the concentrations of the short-chain fatty acids lactic acid, propionic acid, and the signaling molecule indole-3-acetic acid. Microbiome diversity and composition were also predictable from monosaccharide content and SCFA concentration. In particular, the concentrations of lactic acid and propionic acid correlated with final alpha diversity and were significantly associated with the relative abundance of several of the genera, including <i>Lactobacillus</i> and <i>Dubosiella</i>. Our results suggest that monosaccharide composition offers a generalizable method to compare any dietary fiber of interest and uncover links between diet, gut microbiota, and metabolite production.</p><p><strong>Importance: </strong>The survival of a microbial species in the gut depends on the availability of the nutrients necessary for that species to survive. Carbohydrates in the form of non-host digestible fiber are of particular importance, and the set of genes possessed by each species for carbohydrate consumption can vary considerably. Here, differences in the monosaccharides that are the building blocks of fiber are considered for their impact on both the survival of different species of microbes and on the levels of microbial fermentation products produced. This work demonstrates that foods with similar monosaccharide content will have consistent effects on the survival of microbial species and on the production of microbial fermentation products.</p>","PeriodicalId":8002,"journal":{"name":"Applied and Environmental Microbiology","volume":null,"pages":null},"PeriodicalIF":3.9000,"publicationDate":"2024-08-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11337808/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Applied and Environmental Microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/aem.00964-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/7/15 0:00:00","PubModel":"Epub","JCR":"Q2","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Members of the mammalian gut microbiota metabolize diverse complex carbohydrates that are not digested by the host, which are collectively labeled "dietary fiber." While the enzymes and transporters that each strain uses to establish a nutrient niche in the gut are often exquisitely specific, the relationship between carbohydrate structure and microbial ecology is imperfectly understood. The present study takes advantage of recent advances in complex carbohydrate structure determination to test the effects of fiber monosaccharide composition on microbial fermentation. Fifty-five fibers with varied monosaccharide composition were fermented by a pooled feline fecal inoculum in a modified MiniBioReactor array system over a period of 72 hours. The content of the monosaccharides glucose and xylose was significantly associated with the reduction of pH during fermentation, which was also predictable from the concentrations of the short-chain fatty acids lactic acid, propionic acid, and the signaling molecule indole-3-acetic acid. Microbiome diversity and composition were also predictable from monosaccharide content and SCFA concentration. In particular, the concentrations of lactic acid and propionic acid correlated with final alpha diversity and were significantly associated with the relative abundance of several of the genera, including Lactobacillus and Dubosiella. Our results suggest that monosaccharide composition offers a generalizable method to compare any dietary fiber of interest and uncover links between diet, gut microbiota, and metabolite production.

Importance: The survival of a microbial species in the gut depends on the availability of the nutrients necessary for that species to survive. Carbohydrates in the form of non-host digestible fiber are of particular importance, and the set of genes possessed by each species for carbohydrate consumption can vary considerably. Here, differences in the monosaccharides that are the building blocks of fiber are considered for their impact on both the survival of different species of microbes and on the levels of microbial fermentation products produced. This work demonstrates that foods with similar monosaccharide content will have consistent effects on the survival of microbial species and on the production of microbial fermentation products.

膳食纤维单糖含量会改变肠道微生物组的组成和发酵。
哺乳动物肠道微生物群的成员会代谢不被宿主消化的各种复杂碳水化合物,这些碳水化合物被统称为 "膳食纤维"。虽然每个菌株用来在肠道中建立营养龛位的酶和转运体通常都具有极强的特异性,但人们对碳水化合物结构与微生物生态学之间的关系还不完全了解。本研究利用复杂碳水化合物结构测定的最新进展,测试纤维单糖组成对微生物发酵的影响。在改良的 MiniBioReactor 阵列系统中,55 种单糖组成不同的纤维在 72 小时内被汇集的猫粪接种物发酵。单糖葡萄糖和木糖的含量与发酵过程中 pH 值的降低显著相关,这也可以从短链脂肪酸乳酸、丙酸和信号分子吲哚-3-乙酸的浓度中预测出来。单糖含量和 SCFA 浓度也可预测微生物组的多样性和组成。特别是,乳酸和丙酸的浓度与最终的α多样性相关,并与乳酸杆菌和杜博氏菌等几个菌属的相对丰度显著相关。我们的研究结果表明,单糖组成提供了一种通用方法,可用于比较任何感兴趣的膳食纤维,并揭示膳食、肠道微生物群和代谢物产生之间的联系:微生物物种在肠道中的生存取决于该物种生存所需的营养物质的可用性。非宿主可消化纤维形式的碳水化合物尤其重要,而每个物种所拥有的消耗碳水化合物的基因集可能有很大差异。在这里,研究人员考虑了作为纤维组成成分的单糖的差异对不同种类微生物的生存和所产生的微生物发酵产物水平的影响。这项研究表明,单糖含量相似的食物对微生物种类的存活和微生物发酵产物的产生具有一致的影响。
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
Applied and Environmental Microbiology
Applied and Environmental Microbiology 生物-生物工程与应用微生物
CiteScore
7.70
自引率
2.30%
发文量
730
审稿时长
1.9 months
期刊介绍: Applied and Environmental Microbiology (AEM) publishes papers that make significant contributions to (a) applied microbiology, including biotechnology, protein engineering, bioremediation, and food microbiology, (b) microbial ecology, including environmental, organismic, and genomic microbiology, and (c) interdisciplinary microbiology, including invertebrate microbiology, plant microbiology, aquatic microbiology, and geomicrobiology.
×
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