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Unusual molecular architecture of a human gut microbiota β-mannanase reveals a new CBM family
Open accessPreprint — published as 10.1007/s00018-026-06241-x
Abstract
β-mannans are plant structural and storage polysaccharides prevalent in the human diet. Their degradation in the gastrointestinal tract is mediated by the human gut microbiota (HGM) through expression of a plethora of carbohydrate-active enzymes (CAZymes), although our understanding of the details of mannan breakdown is lacking. In this study, a prominent HGM member, Bacteroides cellulosilyticus , was found to be exceptionally efficient at utilising β-mannans, mediated by the expression of a single polysaccharide utilisation locus (PUL). Amongst the predicted surface CAZymes encoded in the PUL, we identified a family 26 glycoside hydrolase of an unusual molecular architecture. Bc WH2_GH26 contains a putative carbohydrate-binding module (CBM) directly intercalated into its catalytic domain, unlike classical CBMs which are located at the N- or C-termini of the catalytic domain. Phylogenetic and functional analyses of this internal CBM, and a homologue from another mannan user Bacteroides uniformis , revealed a narrow specificity for β-mannan and support their classification as a novel CBM family. To investigate the evolutionary basis for the unusual enzyme architecture, the effect of the CBM on the catalytic activity of the enzyme was assessed. No significant differences in the kinetic parameters were found between the full-length and CBM deletion constructs against both soluble and insoluble mannans. The potential role of the internal CBM in enzyme function is discussed in the context of the likely localisation of the Bc WH2_GH26 in the outer membrane utilisome encoded by the Bc mannan PUL.
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Research works printed but not linked: 2
- 2022, Phenotypic and Genomic Diversification in Complex Carbohydrate-Degrading Human Gut Bacteria, mSystems, 7, e00947
- team CD, Boitreaud J , Dent J , McPartlon M , Meier J , Reis V , et al. Chai-1: Decoding the molecular interactions of life. bioRxiv. 2024:2024.10.10.615955.
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Metadata
- Authors
- Łoś, N., Lelėnaitė, I., Willats, W. G. T., Terrapon, N., Morales-García, A. L., Yau, H. C. L., Lowe, E. C., & Bolam, D. N.
- Affiliations
- Newcastle University Biosciences Institute, The Medical School, University of Newcastle Upon Tyne Framlington Place, Newcastle upon Tyne NE2 4HH, UK
- School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK
- Newcastle University (GB)
- Centre National de la Recherche Scientifique (FR)
- Procter & Gamble, Newcastle Innovation Centre, Newcastle upon Tyne NE12 9TS, UK
- Procter & Gamble (United Kingdom) (GB)
- Corresponding author
- Bolam, David N.
- ORCID
- Venue
- Cellular and Molecular Life Sciences
- Publisher
- openRxiv
- Published
- 2026-02-12
- Volume
- 83
- Issue
- 1
- Pages
- 276
- ISSN
- 1420-682X (ISSN-L)
- PMC
- PMC13357471
- OpenAlex
- W7161137552
- Cited by
- 0
- References
- 34
- FWCI
- 0.00
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cellular and Molecular Life Sciences (publishedVersion, cc-by)
- Research Square (acceptedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed (publishedVersion)
- PubMed Central (publishedVersion, cc-by)
- HAL (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- BBSRC and Procter & Gamble
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Enzyme Production and Characterization
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Polysaccharides and Plant Cell Walls
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- β-mannanase, carbohydrate-binding module, Bacteroides cellulosilyticus, Bacteroides uniformis, human gut microbiome, enzyme structure, carbohydrate-active enzymes
- MeSH terms
- Gastrointestinal Microbiome, Carbohydrate Binding Modules, Amino Acid Sequence, Bacterial Proteins, Bacteroides, Humans, Mannans, Phylogeny, Substrate Specificity, Catalytic Domain, beta-Mannosidase
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