Distinct in vitro utilization and degradation of porcine gastric mucin glycans by human intestinal bacteria

Abstract

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.