Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to Bacteroides plebeius

Munoz, Jose, Ndeh, Didier, Fernandez-Julia, Pedro, Walton, Gemma, Henrissat, Bernard, Gilbert, Harry J. and Comstock, Laurie E. (2021) Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to Bacteroides plebeius. mBio, 12 (4). e01368-21. ISSN 2150-7511

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Official URL: https://doi.org/10.1128/mBio.01368-21

Abstract

The human gut microbiota (HGM) contributes to the physiology and health of its host. The health benefits provided by dietary manipulation of the HGM require knowledge of how glycans, the major nutrients available to this ecosystem, are metabolized. Arabinogalactan proteins (AGPs) are a ubiquitous feature of plant polysaccharides available to the HGM. Although the galactan backbone and galactooligosaccharide side chains of AGPs are conserved, the decorations of these structures are highly variable. Here, we tested the hypothesis that these variations in arabinogalactan decoration provide a selection mechanism for specific Bacteroides species within the HGM. The data showed that only a single bacterium, B. plebeius, grew on red wine AGP (Wi-AGP) and seaweed AGP (SW-AGP) in mono- or mixed culture. Wi-AGP thus acts as a privileged nutrient for a Bacteroides species within the HGM that utilizes marine and terrestrial plant glycans. The B. plebeius polysaccharide utilization loci (PULs) upregulated by AGPs encoded a polysaccharide lyase, located in the enzyme family GH145, which hydrolyzed Rha-Glc linkages in Wi-AGP. Further analysis of GH145 identified an enzyme with two active sites that displayed glycoside hydrolase and lyase activities, respectively, which conferred substrate flexibility for different AGPs. The AGP-degrading apparatus of B. plebeius also contained a sulfatase, BpS1_8, active on SW-AGP and Wi-AGP, which played a pivotal role in the utilization of these glycans by the bacterium. BpS1_8 enabled other Bacteroides species to access the sulfated AGPs, providing a route to introducing privileged nutrient utilization into probiotic and commensal organisms that could improve human health.

Item Type: Article
Additional Information: Funding infrormation: The research described in this paper was supported in part by an Advanced Grant from the European Research Council (grant no. 322820) awarded to H.J.G. and B.H. and a Wellcome Trust Senior Investigator Award to H.J.G. (grant no. WT097907MA). These grants supported the work of D.N. and J. M.-M. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Uncontrolled Keywords: Bacteroides, human microbiota, arabinogalactan, glycan-degrading enzymes, microbial ecology, privileged nutrient, sulfatases
Subjects: C500 Microbiology
Department: Faculties > Health and Life Sciences > Applied Sciences
Depositing User: Elena Carlaw
Date Deposited: 12 Aug 2021 09:43
Last Modified: 12 Aug 2021 09:45
URI: http://nrl.northumbria.ac.uk/id/eprint/46898

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