Generation of novel prebiotic oligosaccharide pools from fiber drives biological insight in bacterial glycan metabolism.

IF 3.9 2区 生物学 Q2 BIOTECHNOLOGY & APPLIED MICROBIOLOGY
Applied and Environmental Microbiology Pub Date : 2025-03-19 Epub Date: 2025-02-06 DOI:10.1128/aem.02077-24
Chad Masarweh, Maria Maldonado-Gomez, Bruna Paviani, Mrittika Bhattacharya, Cheng-Yu Weng, Christopher Suarez, Shawn Ehlers-Cheang, Aaron Stacy, Juan Castillo, Nithya Krishnakumar, Karen A Kalanetra, Daniela Barile, J Bruce German, Carlito B Lebrilla, David A Mills
{"title":"Generation of novel prebiotic oligosaccharide pools from fiber drives biological insight in bacterial glycan metabolism.","authors":"Chad Masarweh, Maria Maldonado-Gomez, Bruna Paviani, Mrittika Bhattacharya, Cheng-Yu Weng, Christopher Suarez, Shawn Ehlers-Cheang, Aaron Stacy, Juan Castillo, Nithya Krishnakumar, Karen A Kalanetra, Daniela Barile, J Bruce German, Carlito B Lebrilla, David A Mills","doi":"10.1128/aem.02077-24","DOIUrl":null,"url":null,"abstract":"<p><p>Prebiotic oligosaccharides are dietary supplements that modulate the intestinal gut microbiome by selectively nourishing subsets of the microbial community with a goal to enhance host health. To date, the diversity of polysaccharide compositions in the fiber consumed by humans is not well represented by the limited scope of oligosaccharide compositions present in current commercial prebiotics. Recently, our UC Davis group developed a novel method to generate oligosaccharides from any polysaccharide fiber, termed <u>F</u>enton's <u>I</u>nitiation <u>T</u>oward <u>D</u>efined <u>O</u>ligosaccharide <u>G</u>roups (FITDOG). Using this method, sugar beet pulp (SBP) was transformed into sugar beet oligosaccharides (SBOs) composed of arabinose- and galactose-containing oligosaccharides. Fecal fermentations of SBO and SBP produced similar shifts in donor-specific bacterial communities and acid metabolite profiles with a general enrichment of <i>Bacteroides</i> and <i>Bifidobacterium</i>. However, <i>in vitro</i> tests revealed more <i>Bifidobacterium</i> strains could consume SBO than sugar beet arabinan, and specific strains showed differential consumption of arabinofuranooligosaccharides or galactooligosaccharide (GOS) portions of the SBO pool. Genomic and glycomic comparisons suggest that previously characterized, arabinan-specific, extracellular arabinofuranosidases from <i>Bifidobacterium</i> are not necessary to metabolize the arabino-oligosaccharides within SBO. Synbiotic application of SBO with an SBO-consuming strain <i>Bifidobacterium longum</i> subsp. <i>longum</i> SC596 in serial fecal enrichments resulted in enhanced persistence among 9 of 10 donor feces. This work demonstrates a novel workflow whereby FITDOG creates novel oligosaccharide pools that can provide insight into how compositional differences in fiber drive differential gut fermentation behaviors as well as their downstream health impacts. Moreover, these oligosaccharides may be useful in new prebiotic and synbiotic applications.<b>IMPORTANCE</b>Prebiotics seek to selectively alter the host microbiome composition or function, resulting in a concurrent health benefit to the host. However, commercial prebiotics represent a small fraction of the diversity of food polysaccharide compositions. In this work a novel method, <u>F</u>enton's <u>I</u>nitiation <u>T</u>oward <u>D</u>efined <u>O</u>ligosaccharide <u>G</u>roups (FITDOG) was used to generate an oligosaccharide pool from sugar beet pulp (SBP). Sugar beet oligosaccharides (SBOs) resulted in similar changes to SBP in fecal enrichments; however, SBO could be consumed by more beneficial bifidobacterial strains than the cognate polysaccharide. These results demonstrate how the details of glycan structure have a profound influence on how gut bacteria metabolize food carbohydrates. The implications of this work are relevant to understanding how different dietary sources influence the human microbiome and extend to developing novel oligosaccharide pools for prebiotic applications.</p>","PeriodicalId":8002,"journal":{"name":"Applied and Environmental Microbiology","volume":" ","pages":"e0207724"},"PeriodicalIF":3.9000,"publicationDate":"2025-03-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11921329/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Applied and Environmental Microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/aem.02077-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/2/6 0:00:00","PubModel":"Epub","JCR":"Q2","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Prebiotic oligosaccharides are dietary supplements that modulate the intestinal gut microbiome by selectively nourishing subsets of the microbial community with a goal to enhance host health. To date, the diversity of polysaccharide compositions in the fiber consumed by humans is not well represented by the limited scope of oligosaccharide compositions present in current commercial prebiotics. Recently, our UC Davis group developed a novel method to generate oligosaccharides from any polysaccharide fiber, termed Fenton's Initiation Toward Defined Oligosaccharide Groups (FITDOG). Using this method, sugar beet pulp (SBP) was transformed into sugar beet oligosaccharides (SBOs) composed of arabinose- and galactose-containing oligosaccharides. Fecal fermentations of SBO and SBP produced similar shifts in donor-specific bacterial communities and acid metabolite profiles with a general enrichment of Bacteroides and Bifidobacterium. However, in vitro tests revealed more Bifidobacterium strains could consume SBO than sugar beet arabinan, and specific strains showed differential consumption of arabinofuranooligosaccharides or galactooligosaccharide (GOS) portions of the SBO pool. Genomic and glycomic comparisons suggest that previously characterized, arabinan-specific, extracellular arabinofuranosidases from Bifidobacterium are not necessary to metabolize the arabino-oligosaccharides within SBO. Synbiotic application of SBO with an SBO-consuming strain Bifidobacterium longum subsp. longum SC596 in serial fecal enrichments resulted in enhanced persistence among 9 of 10 donor feces. This work demonstrates a novel workflow whereby FITDOG creates novel oligosaccharide pools that can provide insight into how compositional differences in fiber drive differential gut fermentation behaviors as well as their downstream health impacts. Moreover, these oligosaccharides may be useful in new prebiotic and synbiotic applications.IMPORTANCEPrebiotics seek to selectively alter the host microbiome composition or function, resulting in a concurrent health benefit to the host. However, commercial prebiotics represent a small fraction of the diversity of food polysaccharide compositions. In this work a novel method, Fenton's Initiation Toward Defined Oligosaccharide Groups (FITDOG) was used to generate an oligosaccharide pool from sugar beet pulp (SBP). Sugar beet oligosaccharides (SBOs) resulted in similar changes to SBP in fecal enrichments; however, SBO could be consumed by more beneficial bifidobacterial strains than the cognate polysaccharide. These results demonstrate how the details of glycan structure have a profound influence on how gut bacteria metabolize food carbohydrates. The implications of this work are relevant to understanding how different dietary sources influence the human microbiome and extend to developing novel oligosaccharide pools for prebiotic applications.

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