Cross-Feeding and Enzymatic Catabolism for Mannan-Oligosaccharide Utilization by the Butyrate-Producing Gut Bacterium Roseburia hominis A2-183
(2022) In Microorganisms 10(12).- Abstract
β-Mannan is abundant in the human diet and in hemicellulose derived from softwood. Linear or galactose-substituted β-mannan-oligosaccharides (MOS/GMOSs) derived from β-mannan are considered emerging prebiotics that could stimulate health-associated gut microbiota. However, the underlying mechanisms are not yet resolved. Therefore, this study investigated the cross-feeding and metabolic interactions between Bifidobacterium adolescentis ATCC 15703, an acetate producer, and Roseburia hominis A2-183 DSMZ 16839, a butyrate producer, during utilization of MOS/GMOSs. Cocultivation studies suggest that both strains coexist due to differential MOS/GMOS utilization, along with the cross-feeding of acetate from B. adolescentis E194a to R. hominis... (More)
β-Mannan is abundant in the human diet and in hemicellulose derived from softwood. Linear or galactose-substituted β-mannan-oligosaccharides (MOS/GMOSs) derived from β-mannan are considered emerging prebiotics that could stimulate health-associated gut microbiota. However, the underlying mechanisms are not yet resolved. Therefore, this study investigated the cross-feeding and metabolic interactions between Bifidobacterium adolescentis ATCC 15703, an acetate producer, and Roseburia hominis A2-183 DSMZ 16839, a butyrate producer, during utilization of MOS/GMOSs. Cocultivation studies suggest that both strains coexist due to differential MOS/GMOS utilization, along with the cross-feeding of acetate from B. adolescentis E194a to R. hominis A2-183. The data suggest that R. hominis A2-183 efficiently utilizes MOS/GMOS in mono- and cocultivation. Notably, we observed the transcriptional upregulation of certain genes within a dedicated MOS/GMOS utilization locus (RhMosUL), and an exo-oligomannosidase (RhMan113A) gene located distally in the R. hominis A2-183 genome. Significantly, biochemical analysis of β-1,4 mannan-oligosaccharide phosphorylase (RhMOP130A), α-galactosidase (RhGal36A), and exo-oligomannosidase (RhMan113A) suggested their potential synergistic role in the initial utilization of MOS/GMOSs. Thus, our results enhance the understanding of MOS/GMOS utilization by potential health-promoting human gut microbiota and highlight the role of cross-feeding and metabolic interactions between two secondary mannan degraders inhabiting the same ecological niche in the gut.
(Less)
- author
- Bhattacharya, Abhishek LU ; Majtorp, Lovisa LU ; Birgersson, Simon LU ; Wiemann, Mathias LU ; Sreenivas, Krishnan LU ; Verbrugghe, Phebe LU ; Aken, Olivier Van LU ; Niel, Ed W.J.Van LU and Stålbrand, Henrik LU
- organization
- publishing date
- 2022-12
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- Bifidobacterium adolescentis, butyrate production, cocultivation, cross-feeding, differential gene expression, exo-oligomannosidase, Roseburia hominis, α-galactosidase, β-1,4 mannan-oligosaccharide phosphorylase, β-mannan-oligosaccharides
- in
- Microorganisms
- volume
- 10
- issue
- 12
- article number
- 2496
- publisher
- MDPI AG
- external identifiers
-
- scopus:85144700483
- pmid:36557749
- ISSN
- 2076-2607
- DOI
- 10.3390/microorganisms10122496
- language
- English
- LU publication?
- yes
- id
- 78cb3e3c-b8e7-4bd1-b979-8d09757d5cfc
- date added to LUP
- 2023-01-05 12:13:12
- date last changed
- 2024-06-13 22:51:07
@article{78cb3e3c-b8e7-4bd1-b979-8d09757d5cfc,
abstract = {{<p>β-Mannan is abundant in the human diet and in hemicellulose derived from softwood. Linear or galactose-substituted β-mannan-oligosaccharides (MOS/GMOSs) derived from β-mannan are considered emerging prebiotics that could stimulate health-associated gut microbiota. However, the underlying mechanisms are not yet resolved. Therefore, this study investigated the cross-feeding and metabolic interactions between Bifidobacterium adolescentis ATCC 15703, an acetate producer, and Roseburia hominis A2-183 DSMZ 16839, a butyrate producer, during utilization of MOS/GMOSs. Cocultivation studies suggest that both strains coexist due to differential MOS/GMOS utilization, along with the cross-feeding of acetate from B. adolescentis E194a to R. hominis A2-183. The data suggest that R. hominis A2-183 efficiently utilizes MOS/GMOS in mono- and cocultivation. Notably, we observed the transcriptional upregulation of certain genes within a dedicated MOS/GMOS utilization locus (RhMosUL), and an exo-oligomannosidase (RhMan113A) gene located distally in the R. hominis A2-183 genome. Significantly, biochemical analysis of β-1,4 mannan-oligosaccharide phosphorylase (RhMOP130A), α-galactosidase (RhGal36A), and exo-oligomannosidase (RhMan113A) suggested their potential synergistic role in the initial utilization of MOS/GMOSs. Thus, our results enhance the understanding of MOS/GMOS utilization by potential health-promoting human gut microbiota and highlight the role of cross-feeding and metabolic interactions between two secondary mannan degraders inhabiting the same ecological niche in the gut.</p>}},
author = {{Bhattacharya, Abhishek and Majtorp, Lovisa and Birgersson, Simon and Wiemann, Mathias and Sreenivas, Krishnan and Verbrugghe, Phebe and Aken, Olivier Van and Niel, Ed W.J.Van and Stålbrand, Henrik}},
issn = {{2076-2607}},
keywords = {{Bifidobacterium adolescentis; butyrate production; cocultivation; cross-feeding; differential gene expression; exo-oligomannosidase; Roseburia hominis; α-galactosidase; β-1,4 mannan-oligosaccharide phosphorylase; β-mannan-oligosaccharides}},
language = {{eng}},
number = {{12}},
publisher = {{MDPI AG}},
series = {{Microorganisms}},
title = {{Cross-Feeding and Enzymatic Catabolism for Mannan-Oligosaccharide Utilization by the Butyrate-Producing Gut Bacterium Roseburia hominis A2-183}},
url = {{http://dx.doi.org/10.3390/microorganisms10122496}},
doi = {{10.3390/microorganisms10122496}},
volume = {{10}},
year = {{2022}},
}