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Singh, Ravindra Pal, Niharika, Jayashree, Thakur, Raksha, Wagstaff, Ben A., Kumar, Gulshan, Kurata, Rikuya, Patel, Dhaval, Levy, Colin W., Miyazaki, Takatsugu and Field, Robert A. 
ORCID: https://orcid.org/0000-0001-8574-0275
(2023)
Utilization of dietary mixed-linkage β-glucans by the Firmicute Blautia producta.
Journal of Biological Chemistry, 299 (6).
ISSN 0021-9258
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Abstract
The β-glucans are structurally varied, naturally occurring components of the cell walls, and storage materials of a variety of plant and microbial species. In the human diet, mixed-linkage glucans [MLG - β-(1,3/4)-glucans] influence the gut microbiome and the host immune system. Although consumed daily, the molecular mechanism by which human gut Gram-positive bacteria utilize MLG largely remains unknown. In this study, we used Blautia producta ATCC 27340 as a model organism to develop an understanding of MLG utilization. B. producta encodes a gene locus comprising a multi-modular cell-anchored endo-glucanase (BpGH16MLG), an ABC transporter, and a glycoside phosphorylase (BpGH94MLG) for utilizing MLG, as evidenced by the upregulation of expression of the enzyme- and solute binding protein (SBP)–encoding genes in this cluster when the organism is grown on MLG. We determined that recombinant BpGH16MLG cleaved various types of β-glucan, generating oligosaccharides suitable for cellular uptake by B. producta. Cytoplasmic digestion of these oligosaccharides is then performed by recombinant BpGH94MLG and β-glucosidases (BpGH3-AR8MLG and BpGH3-X62MLG). Using targeted deletion, we demonstrated BpSBPMLG is essential for B. producta growth on barley β-glucan. Furthermore, we revealed that beneficial bacteria, such as Roseburia faecis JCM 17581T, Bifidobacterium pseudocatenulatum JCM 1200T, Bifidobacterium adolescentis JCM 1275T, and Bifidobacterium bifidum JCM 1254, can also utilize oligosaccharides resulting from the action of BpGH16MLG. Disentangling the β-glucan utilizing the capability of B. producta provides a rational basis on which to consider the probiotic potential of this class of organism.
| Item Type: | Article |
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| Additional Information: | Data availability statement: Structure factors and atomic coordinates of BpGH94MLG have been deposited with the Protein Data Bank with accession code; PDB ID 8BOU. All other data are provided either in the Supporting information or can be available from the corresponding author upon reasonable request. Funding Information: R. P. Singh would like to thank the Department of Biotechnology, India for providing the Ramalingaswami Re-entry Fellowship and Grant in-aid-number: BT/PR32876/PFN/20/1471/2020 and BT/PR38298/PFN/20/1558/2020. The authors would like to thank Dr Vikas Rishi from NABI, Mohali for assisting with circular dichroism (CD) spectroscopy analysis. The authors would like to thank the Diamond Light Source for beam-time on i03 (proposal mx24447-60). The University of Manchester is acknowledged for providing financial support. |
| Uncontrolled Keywords: | blautia producta,glucan hydrolase,glucan phosphorylase,metabolism,mixed-linkage β-glucan (mlg),biochemistry,molecular biology,cell biology ,/dk/atira/pure/subjectarea/asjc/1300/1303 |
| Faculty \ School: | Faculty of Science > School of Chemistry, Pharmacy and Pharmacology |
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| Depositing User: | LivePure Connector |
| Date Deposited: | 03 Sep 2024 15:34 |
| Last Modified: | 02 Oct 2024 09:30 |
| URI: | https://ueaeprints.uea.ac.uk/id/eprint/96478 |
| DOI: | 10.1016/j.jbc.2023.104806 |
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