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Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut

Responses of the microbiota to diet are highly personalized but mechanistically not well understood because many metabolic capabilities and interactions of human gut microorganisms are unknown. Here we show that sulfoquinovose (SQ), a sulfonated monosaccharide omnipresent in green vegetables, is a s...

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Autores principales: Hanson, Buck T., Dimitri Kits, K., Löffler, Jessica, Burrichter, Anna G., Fiedler, Alexander, Denger, Karin, Frommeyer, Benjamin, Herbold, Craig W., Rattei, Thomas, Karcher, Nicolai, Segata, Nicola, Schleheck, David, Loy, Alexander
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8397734/
https://www.ncbi.nlm.nih.gov/pubmed/33790426
http://dx.doi.org/10.1038/s41396-021-00968-0
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author Hanson, Buck T.
Dimitri Kits, K.
Löffler, Jessica
Burrichter, Anna G.
Fiedler, Alexander
Denger, Karin
Frommeyer, Benjamin
Herbold, Craig W.
Rattei, Thomas
Karcher, Nicolai
Segata, Nicola
Schleheck, David
Loy, Alexander
author_facet Hanson, Buck T.
Dimitri Kits, K.
Löffler, Jessica
Burrichter, Anna G.
Fiedler, Alexander
Denger, Karin
Frommeyer, Benjamin
Herbold, Craig W.
Rattei, Thomas
Karcher, Nicolai
Segata, Nicola
Schleheck, David
Loy, Alexander
author_sort Hanson, Buck T.
collection PubMed
description Responses of the microbiota to diet are highly personalized but mechanistically not well understood because many metabolic capabilities and interactions of human gut microorganisms are unknown. Here we show that sulfoquinovose (SQ), a sulfonated monosaccharide omnipresent in green vegetables, is a selective yet relevant substrate for few but ubiquitous bacteria in the human gut. In human feces and in defined co-culture, Eubacterium rectale and Bilophila wadsworthia used recently identified pathways to cooperatively catabolize SQ with 2,3-dihydroxypropane-1-sulfonate as a transient intermediate to hydrogen sulfide (H(2)S), a key intestinal metabolite with disparate effects on host health. SQ-degradation capability is encoded in almost half of E. rectale genomes but otherwise sparsely distributed among microbial species in the human intestine. However, re-analysis of fecal metatranscriptome datasets of four human cohorts showed that SQ degradation (mostly from E. rectale and Faecalibacterium prausnitzii) and H(2)S production (mostly from B. wadsworthia) pathways were expressed abundantly across various health states, demonstrating that these microbial functions are core attributes of the human gut. The discovery of green-diet-derived SQ as an exclusive microbial nutrient and an additional source of H(2)S in the human gut highlights the role of individual dietary compounds and organosulfur metabolism on microbial activity and has implications for precision editing of the gut microbiota by dietary and prebiotic interventions.
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spelling pubmed-83977342021-09-15 Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut Hanson, Buck T. Dimitri Kits, K. Löffler, Jessica Burrichter, Anna G. Fiedler, Alexander Denger, Karin Frommeyer, Benjamin Herbold, Craig W. Rattei, Thomas Karcher, Nicolai Segata, Nicola Schleheck, David Loy, Alexander ISME J Article Responses of the microbiota to diet are highly personalized but mechanistically not well understood because many metabolic capabilities and interactions of human gut microorganisms are unknown. Here we show that sulfoquinovose (SQ), a sulfonated monosaccharide omnipresent in green vegetables, is a selective yet relevant substrate for few but ubiquitous bacteria in the human gut. In human feces and in defined co-culture, Eubacterium rectale and Bilophila wadsworthia used recently identified pathways to cooperatively catabolize SQ with 2,3-dihydroxypropane-1-sulfonate as a transient intermediate to hydrogen sulfide (H(2)S), a key intestinal metabolite with disparate effects on host health. SQ-degradation capability is encoded in almost half of E. rectale genomes but otherwise sparsely distributed among microbial species in the human intestine. However, re-analysis of fecal metatranscriptome datasets of four human cohorts showed that SQ degradation (mostly from E. rectale and Faecalibacterium prausnitzii) and H(2)S production (mostly from B. wadsworthia) pathways were expressed abundantly across various health states, demonstrating that these microbial functions are core attributes of the human gut. The discovery of green-diet-derived SQ as an exclusive microbial nutrient and an additional source of H(2)S in the human gut highlights the role of individual dietary compounds and organosulfur metabolism on microbial activity and has implications for precision editing of the gut microbiota by dietary and prebiotic interventions. Nature Publishing Group UK 2021-03-31 2021-09 /pmc/articles/PMC8397734/ /pubmed/33790426 http://dx.doi.org/10.1038/s41396-021-00968-0 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Hanson, Buck T.
Dimitri Kits, K.
Löffler, Jessica
Burrichter, Anna G.
Fiedler, Alexander
Denger, Karin
Frommeyer, Benjamin
Herbold, Craig W.
Rattei, Thomas
Karcher, Nicolai
Segata, Nicola
Schleheck, David
Loy, Alexander
Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut
title Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut
title_full Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut
title_fullStr Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut
title_full_unstemmed Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut
title_short Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut
title_sort sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide in the human gut
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8397734/
https://www.ncbi.nlm.nih.gov/pubmed/33790426
http://dx.doi.org/10.1038/s41396-021-00968-0
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