Distinct <i>in vitro</i> utilization and degradation of porcine gastric mucin glycans by human intestinal bacteria

Mucin glycan degradation and utilization by microbes colonizing the human intestine is an essential host-microbe interaction. In this study, degradation and utilization of porcine gastric mucin glycans by Akkermansia muciniphila, Ruminococcus torques, Bacteroides thetaiotaomicron, co-cultures, and a synthetic bacterial community were investigated over time. Liquid chromatography-tandem mass spectrometry O-glycan patterns revealed that all three monocultures removed sialic acid residues. Furthermore, R. torques first targeted fucosylated O-glycans, while A. muciniphila and B. thetaiotaomicron equally favoured fucosylated and non-fucosylated O-glycans. A. muciniphila, R. torques, and B. thetaiotaomicron favoured degradation of first core 2 O-glycan structures relative to core 1 O-glycan structures. Co-cultures, compared to monocultures, demonstrated different O-glycan degradation patterns suggesting distinct ecological interactions between the bacteria. Although extensive O-glycan degradation was observed by the monocultures and co-cultures, only the synthetic community completely degraded all O-glycans within 24 h. Regarding degradation of the constituent N-glycans, matrix-assisted laser desorption ionization-time-of-flight mass spectrometry showed that A. muciniphila and R. torques can partly degrade N-glycans, B. thetaiotaomicron can completely degrade high-mannose N-glycans, and the synthetic community can degrade all N-glycans. The utilization of mucin glycans was observed by production of different metabolites among the bacteria. These results indicate that degradation of mucin glycans depends on microbial interactions and ecological networks.