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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
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.
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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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