Hierarchical glycolytic pathways control the carbohydrate utilization regulator in human gut Bacteroides

Abstract Human dietary choices control the gut microbiome. Industrialized populations consume abundant amounts of glucose and fructose, resulting in microbe-dependent intestinal disorders. Simple sugars inhibit the carbohydrate utilization regulator (Cur), a transcription factor in members of the pr...

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Main Authors: Seth G. Kabonick, Kamalesh Verma, Jennifer L. Modesto, Victoria H. Pearce, Kailyn M. Winokur, Eduardo A. Groisman, Guy E. Townsend
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-59704-3
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author Seth G. Kabonick
Kamalesh Verma
Jennifer L. Modesto
Victoria H. Pearce
Kailyn M. Winokur
Eduardo A. Groisman
Guy E. Townsend
author_facet Seth G. Kabonick
Kamalesh Verma
Jennifer L. Modesto
Victoria H. Pearce
Kailyn M. Winokur
Eduardo A. Groisman
Guy E. Townsend
author_sort Seth G. Kabonick
collection DOAJ
description Abstract Human dietary choices control the gut microbiome. Industrialized populations consume abundant amounts of glucose and fructose, resulting in microbe-dependent intestinal disorders. Simple sugars inhibit the carbohydrate utilization regulator (Cur), a transcription factor in members of the prominent gut bacterial phylum, Bacteroidetes. Cur controls products necessary for carbohydrate utilization, host immunomodulation, and intestinal colonization. Here, we demonstrate how simple sugars decrease Cur activity in the mammalian gut. Our findings in two Bacteroides species show that ATP-dependent fructose-1,6-bisphosphate (FBP) synthesis is necessary for glucose or fructose to inhibit Cur, but dispensable for growth because of an essential pyrophosphate (PPi)-dependent enzyme. Furthermore, we show that ATP-dependent FBP synthesis is required to regulate Cur in the gut but does not contribute to fitness when cur is absent, indicating PPi is sufficient to drive glycolysis in these bacteria. Our findings reveal how sugar-rich diets inhibit Cur, thereby disrupting Bacteroides fitness and diminishing products that are beneficial to the host.
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publishDate 2025-05-01
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spelling doaj-art-d8e02df1fd2a4dcf903b7ece1e4acf102025-08-20T02:25:16ZengNature PortfolioNature Communications2041-17232025-05-0116111010.1038/s41467-025-59704-3Hierarchical glycolytic pathways control the carbohydrate utilization regulator in human gut BacteroidesSeth G. Kabonick0Kamalesh Verma1Jennifer L. Modesto2Victoria H. Pearce3Kailyn M. Winokur4Eduardo A. Groisman5Guy E. Townsend6Penn State College of MedicinePenn State College of MedicinePenn State College of MedicinePenn State College of MedicinePenn State College of MedicineYale University School of MedicinePenn State College of MedicineAbstract Human dietary choices control the gut microbiome. Industrialized populations consume abundant amounts of glucose and fructose, resulting in microbe-dependent intestinal disorders. Simple sugars inhibit the carbohydrate utilization regulator (Cur), a transcription factor in members of the prominent gut bacterial phylum, Bacteroidetes. Cur controls products necessary for carbohydrate utilization, host immunomodulation, and intestinal colonization. Here, we demonstrate how simple sugars decrease Cur activity in the mammalian gut. Our findings in two Bacteroides species show that ATP-dependent fructose-1,6-bisphosphate (FBP) synthesis is necessary for glucose or fructose to inhibit Cur, but dispensable for growth because of an essential pyrophosphate (PPi)-dependent enzyme. Furthermore, we show that ATP-dependent FBP synthesis is required to regulate Cur in the gut but does not contribute to fitness when cur is absent, indicating PPi is sufficient to drive glycolysis in these bacteria. Our findings reveal how sugar-rich diets inhibit Cur, thereby disrupting Bacteroides fitness and diminishing products that are beneficial to the host.https://doi.org/10.1038/s41467-025-59704-3
spellingShingle Seth G. Kabonick
Kamalesh Verma
Jennifer L. Modesto
Victoria H. Pearce
Kailyn M. Winokur
Eduardo A. Groisman
Guy E. Townsend
Hierarchical glycolytic pathways control the carbohydrate utilization regulator in human gut Bacteroides
Nature Communications
title Hierarchical glycolytic pathways control the carbohydrate utilization regulator in human gut Bacteroides
title_full Hierarchical glycolytic pathways control the carbohydrate utilization regulator in human gut Bacteroides
title_fullStr Hierarchical glycolytic pathways control the carbohydrate utilization regulator in human gut Bacteroides
title_full_unstemmed Hierarchical glycolytic pathways control the carbohydrate utilization regulator in human gut Bacteroides
title_short Hierarchical glycolytic pathways control the carbohydrate utilization regulator in human gut Bacteroides
title_sort hierarchical glycolytic pathways control the carbohydrate utilization regulator in human gut bacteroides
url https://doi.org/10.1038/s41467-025-59704-3
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