Sulfation of Arabinogalactan Proteins Confers Privileged Nutrient Status to Bacteroides plebeius

• Published in: mBio Vol. 12; no. 4; p. e0136821
• Main Authors: Munoz-Munoz, Jose, Ndeh, Didier, Fernandez-Julia, Pedro, Walton, Gemma, Henrissat, Bernard, Gilbert, Harry J
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 31.08.2021
• Subjects: arabinogalactan; Bacteroides; Bacteroides - enzymology; Bacteroides - genetics; Bacteroides - growth & development; Bacteroides - metabolism; Dietary Carbohydrates - metabolism; Gastrointestinal Microbiome - physiology; glycan-degrading enzymes; human microbiota; microbial ecology; Mucoproteins - metabolism; Nutrients - metabolism; Plant Proteins - metabolism; Polysaccharide-Lyases - genetics; Polysaccharide-Lyases - metabolism; Polysaccharides - metabolism; privileged nutrient; Research Article; Sulfatases - metabolism; glycan-degrading enzymes; privileged nutrient; arabinogalactan; sulfatases; microbial ecology; Bacteroides; human microbiota
• ISSN: 2150-7511; 2150-7511
• DOI: 10.1128/mbio.01368-21

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 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 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 species to access the sulfated AGPs, providing a route to introducing privileged nutrient utilization into probiotic and commensal organisms that could improve human health. Dietary manipulation of the HGM requires knowledge of how glycans available to this ecosystem are metabolized. The variable structures that decorate the core component of plant AGPs may influence their utilization by specific organisms within the HGM. Here, we evaluated the ability of species to utilize a marine and terrestrial AGP. The data showed that a single bacterium, B. plebeius, grew on Wi-AGP and SW-AGP in mono- or mixed culture. Wi-AGP is thus a privileged nutrient for a species that utilizes marine and terrestrial plant glycans. A key component of the AGP-degrading apparatus of B. plebeius is a sulfatase that conferred the ability of the bacterium to utilize these glycans. The enzyme enabled other species to access the sulfated AGPs, providing a route to introducing privileged nutrient utilization into probiotic and commensal organisms that could improve human health.