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Human Gut Faecalibacterium prausnitzii Deploys a Highly Efficient Conserved System To Cross-Feed on β-Mannan-Derived Oligosaccharides
β-Mannans are hemicelluloses that are abundant in modern diets as components in seed endosperms and common additives in processed food. Currently, the collective understanding of β-mannan saccharification in the human colon is limited to a few keystone species, which presumably liberate low-molecula...
Autores principales: | , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8262883/ https://www.ncbi.nlm.nih.gov/pubmed/34061597 http://dx.doi.org/10.1128/mBio.03628-20 |
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author | Lindstad, Lars J. Lo, Galiana Leivers, Shaun Lu, Zijia Michalak, Leszek Pereira, Gabriel V. Røhr, Åsmund K. Martens, Eric C. McKee, Lauren S. Louis, Petra Duncan, Sylvia H. Westereng, Bjørge Pope, Phillip B. La Rosa, Sabina Leanti |
author_facet | Lindstad, Lars J. Lo, Galiana Leivers, Shaun Lu, Zijia Michalak, Leszek Pereira, Gabriel V. Røhr, Åsmund K. Martens, Eric C. McKee, Lauren S. Louis, Petra Duncan, Sylvia H. Westereng, Bjørge Pope, Phillip B. La Rosa, Sabina Leanti |
author_sort | Lindstad, Lars J. |
collection | PubMed |
description | β-Mannans are hemicelluloses that are abundant in modern diets as components in seed endosperms and common additives in processed food. Currently, the collective understanding of β-mannan saccharification in the human colon is limited to a few keystone species, which presumably liberate low-molecular-weight mannooligosaccharide fragments that become directly available to the surrounding microbial community. Here, we show that a dominant butyrate producer in the human gut, Faecalibacterium prausnitzii, is able to acquire and degrade various β-mannooligosaccharides (β-MOS), which are derived by the primary mannanolytic activity of neighboring gut microbiota. Detailed biochemical analyses of selected protein components from their two β-MOS utilization loci (F. prausnitzii β-MOS utilization loci [FpMULs]) supported a concerted model whereby the imported β-MOS are stepwise disassembled intracellularly by highly adapted enzymes. Coculturing experiments of F. prausnitzii with the primary degraders Bacteroides ovatus and Roseburia intestinalis on polymeric β-mannan resulted in syntrophic growth, thus confirming the high efficiency of the FpMULs’ uptake system. Genomic comparison with human F. prausnitzii strains and analyses of 2,441 public human metagenomes revealed that FpMULs are highly conserved and distributed worldwide. Together, our results provide a significant advance in the knowledge of β-mannan metabolism and the degree to which its degradation is mediated by cross-feeding interactions between prominent beneficial microbes in the human gut. |
format | Online Article Text |
id | pubmed-8262883 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-82628832021-07-23 Human Gut Faecalibacterium prausnitzii Deploys a Highly Efficient Conserved System To Cross-Feed on β-Mannan-Derived Oligosaccharides Lindstad, Lars J. Lo, Galiana Leivers, Shaun Lu, Zijia Michalak, Leszek Pereira, Gabriel V. Røhr, Åsmund K. Martens, Eric C. McKee, Lauren S. Louis, Petra Duncan, Sylvia H. Westereng, Bjørge Pope, Phillip B. La Rosa, Sabina Leanti mBio Research Article β-Mannans are hemicelluloses that are abundant in modern diets as components in seed endosperms and common additives in processed food. Currently, the collective understanding of β-mannan saccharification in the human colon is limited to a few keystone species, which presumably liberate low-molecular-weight mannooligosaccharide fragments that become directly available to the surrounding microbial community. Here, we show that a dominant butyrate producer in the human gut, Faecalibacterium prausnitzii, is able to acquire and degrade various β-mannooligosaccharides (β-MOS), which are derived by the primary mannanolytic activity of neighboring gut microbiota. Detailed biochemical analyses of selected protein components from their two β-MOS utilization loci (F. prausnitzii β-MOS utilization loci [FpMULs]) supported a concerted model whereby the imported β-MOS are stepwise disassembled intracellularly by highly adapted enzymes. Coculturing experiments of F. prausnitzii with the primary degraders Bacteroides ovatus and Roseburia intestinalis on polymeric β-mannan resulted in syntrophic growth, thus confirming the high efficiency of the FpMULs’ uptake system. Genomic comparison with human F. prausnitzii strains and analyses of 2,441 public human metagenomes revealed that FpMULs are highly conserved and distributed worldwide. Together, our results provide a significant advance in the knowledge of β-mannan metabolism and the degree to which its degradation is mediated by cross-feeding interactions between prominent beneficial microbes in the human gut. American Society for Microbiology 2021-06-01 /pmc/articles/PMC8262883/ /pubmed/34061597 http://dx.doi.org/10.1128/mBio.03628-20 Text en Copyright © 2021 Lindstad et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Lindstad, Lars J. Lo, Galiana Leivers, Shaun Lu, Zijia Michalak, Leszek Pereira, Gabriel V. Røhr, Åsmund K. Martens, Eric C. McKee, Lauren S. Louis, Petra Duncan, Sylvia H. Westereng, Bjørge Pope, Phillip B. La Rosa, Sabina Leanti Human Gut Faecalibacterium prausnitzii Deploys a Highly Efficient Conserved System To Cross-Feed on β-Mannan-Derived Oligosaccharides |
title | Human Gut Faecalibacterium prausnitzii Deploys a Highly Efficient Conserved System To Cross-Feed on β-Mannan-Derived Oligosaccharides |
title_full | Human Gut Faecalibacterium prausnitzii Deploys a Highly Efficient Conserved System To Cross-Feed on β-Mannan-Derived Oligosaccharides |
title_fullStr | Human Gut Faecalibacterium prausnitzii Deploys a Highly Efficient Conserved System To Cross-Feed on β-Mannan-Derived Oligosaccharides |
title_full_unstemmed | Human Gut Faecalibacterium prausnitzii Deploys a Highly Efficient Conserved System To Cross-Feed on β-Mannan-Derived Oligosaccharides |
title_short | Human Gut Faecalibacterium prausnitzii Deploys a Highly Efficient Conserved System To Cross-Feed on β-Mannan-Derived Oligosaccharides |
title_sort | human gut faecalibacterium prausnitzii deploys a highly efficient conserved system to cross-feed on β-mannan-derived oligosaccharides |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8262883/ https://www.ncbi.nlm.nih.gov/pubmed/34061597 http://dx.doi.org/10.1128/mBio.03628-20 |
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