Fucosylated Human Milk Oligosaccharide Foraging within the Species Bifidobacterium pseudocatenulatum Is Driven by Glycosyl Hydrolase Content and Specificity

Guy Shani, Jennifer L. Hoeflinger, Britta E. Heiss, Chad F. Masarweh, Jules A. Larke, Nick M. Jensen, Saumya Wickramasinghe, Jasmine C. Davis, Elisha Goonatilleke, Amr El-Hawiet, Linh Nguyen, John S. Klassen, Carolyn M. Slupsky, Carlito B. Lebrilla, David A. Mills

Research output: Contribution to journalArticlepeer-review

Abstract

Human milk enriches members of the genus Bifidobacterium in the infant gut. One species, Bifidobacterium pseudocatenulatum, is found in the gastrointestinal tracts of adults and breastfed infants. In this study, B. pseudocatenulatum strains were isolated and characterized to identify genetic adaptations to the breastfed infant gut. During growth on pooled human milk oligosaccharides (HMOs), we observed two distinct groups of B. pseudocatenulatum, isolates that readily consumed HMOs and those that did not, a difference driven by variable catabolism of fucosylated HMOs. A conserved gene cluster for fucosylated HMO utilization was identified in several sequenced B. pseudocatenulatum strains. One isolate, B. pseudocatenulatum MP80, which uniquely possessed GH95 and GH29 a-fucosidases, consumed the majority of fucosylated HMOs tested. Furthermore, B. pseudocatenulatum SC585, which possesses only a single GH95 a-fucosidase, lacked the ability to consume the complete repertoire of linkages within the fucosylated HMO pool. Analysis of the purified GH29 and GH95 fucosidase activities directly on HMOs revealed complementing enzyme specificities with the GH95 enzyme preferring 1-2 fucosyl linkages and the GH29 enzyme favoring 1-3 and 1-4 linkages. The HMO-binding specificities of the family 1 solute-binding protein component linked to the fucosylated HMO gene cluster in both SC585 and MP80 are similar, suggesting differential transport of fucosylated HMO is not a driving factor in each strain's distinct HMO consumption pattern. Taken together, these data indicate the presence or absence of specific a-fucosidases directs the strain-specific fucosylated HMO utilization pattern among bifidobacteria and likely influences competitive behavior for HMO foraging in situ.

Original languageEnglish (US)
Article numbere01707-21
JournalApplied and environmental microbiology
Volume88
Issue number2
DOIs
StatePublished - Jan 2022

Keywords

  • A-fucosidase
  • Bifidobacterium
  • Bifidobacterium pseudocatenulatum
  • Fucosidases
  • Fucosylated HMO
  • Glycan metabolism
  • Milk oligosaccharides
  • Strain specificity
  • Substrate-binding protein

ASJC Scopus subject areas

  • Biotechnology
  • Food Science
  • Ecology
  • Applied Microbiology and Biotechnology

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