Glycans, the major source of energy for the human gut microbiota (HGM), are metabolised by numerous members of the Bacteroides genus. Arabinogalactan proteins (AGPs) are a ubiquitous and highly heterogenous group of plant glycans in which a B1,3-galactan backbone and B1,6-galactan side chains are conserved features. Diversity is provided by the extensive and highly variable nature of the sugars that decorate both the backbone and side chain galactans. The mechanisms by which nutritionally relevant AGPs are degraded at a cellular and biochemical level are poorly understood, as is the impact of this process on the ecology of the HGM. Here we have explored how the HGM organism Bacteroides thetaiotaomicron metabolises simple and highly complex AGPs. We propose a sequential degradative model in which a repertoire of exo-acting family GH43 B1,3-galactanases releases backbone galactose units that are attached to the side chains. The oligosaccharide side chains are depolymerized by the synergistic action of exo-acting enzymes in which catalytic interactions are dependent on whether degradation is initiated by a lyase or glycoside hydrolase. We identified an a-L-arabinofuranosidase and B-D-glucuronidase that are the founders of two previously undiscovered glycoside hydrolase families. The crystal structures of the backbone exo-B1,3-galactanases identified a key specificity determinant and reveals significant departure from the canonical catalytic apparatus of other family GH43 enzymes. Growth studies of 20 HGM Bacteroidetes species on a complex AGP revealed three keystone organisms that facilitated utilisation of fragments of the glycan by the 17 other bacteria, which thus acted as recipients. The ability to function as a keystone organism was conferred by a surface endo-B1,3-galactanase, which, when engineered into a recipient enabled this bacterium to utilise complex AGPs and facilitate the growth of the other Bacteroidetes species. This study underpins future pre- and probiotic strategies to exploit AGPs to manipulate the function of the HGM.