Utilization Efficiency of Human Milk Oligosaccharides by Human-Associated Akkermansia Is Strain Dependent

Estefani Luna, Shanthi G. Parkar, Nina Kirmiz, Stephanie Hartel, Erik Hearn, Marziiah Hossine, Arinnae Kurdian, Claudia Mendoza, Katherine Orr, Loren Padilla, Katherine Ramirez, Priscilla Salcedo, Erik Serrano, Biswa Choudhury, Mousumi Paulchakrabarti, Craig T. Parker, Steven Huynh, Kerry Cooper, Gilberto E. Flores

Research output: Contribution to journalArticlepeer-review

40 Scopus citations

Abstract

Akkermansia muciniphila is a mucin-degrading bacterium found in the human gut and is often associated with positive human health. However, despite being detected by as early as 1 month of age, little is known about the role of Akkermansia in the infant gut. Human milk oligosaccharides (HMOs) are abundant components of human milk and are structurally similar to the oligosaccharides that comprise mucin, the preferred growth substrate of human-associated Akkermansia. A limited subset of intestinal bacteria has been shown to grow well on HMOs and mucin. We therefore examined the ability of genomically diverse strains of Akkermansia to grow on HMOs. First, we screened 85 genomes representing the four known Akkermansia phylogroups to examine their metabolic potential to degrade HMOs. Furthermore, we examined the ability of representative isolates to grow on individual HMOs in a mucin background and analyzed the resulting metabolites. All Akkermansia genomes were equipped with an array of glycoside hydrolases associated with HMO deconstruction. Representative strains were all able to grow on HMOs with various efficiencies and growth yields. Strain CSUN-19, belonging to the AmIV phylogroup, grew to the highest level in the presence of fucosylated and sialylated HMOs. This activity may be partially related to the increased copy numbers and/or the enzyme activities of the α-fucosidases, α-sialidases, and β-galactosidases. This study examines the utilization of individual purified HMOs by Akkermansia strains representing all known phylogroups. Further studies are required to examine how HMO ingestion influences gut microbial ecology in infants harboring different Akkermansia phylogroups.

Original languageEnglish (US)
Article numbere01487-21
JournalApplied and environmental microbiology
Volume88
Issue number1
DOIs
StatePublished - Jan 2022

Keywords

  • Akkermansia muciniphila
  • Akkermansia phylogroups
  • Fucosylated HMO
  • GH29
  • GH95
  • Glycoside hydrolase (GH)
  • HMO utilization
  • Human milk oligosaccharides
  • Sialylated HMO

ASJC Scopus subject areas

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

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