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Akkermansia muciniphila uses human milk oligosaccharides to thrive in the early life conditions in vitro.

ABSTRACT: Akkermansia muciniphila is a well-studied anaerobic bacterium specialized in mucus degradation and associated with human health. Because of the structural resemblance of mucus glycans and free human milk oligosaccharides (HMOs), we studied the ability of A. muciniphila to utilize human milk oligosaccharides. We found that A. muciniphila was able to grow on human milk and degrade HMOs. Analyses of the proteome of A. muciniphila indicated that key-glycan degrading enzymes were expressed when the bacterium was grown on human milk. Our results display the functionality of the key-glycan degrading enzymes (?-L-fucosidases, ?-galactosidases, exo-?-sialidases and ?-acetylhexosaminidases) to degrade the HMO-structures 2'-FL, LNT, lactose, and LNT2. The hydrolysation of the host-derived glycan structures allows A. muciniphila to promote syntrophy with other beneficial bacteria, contributing in that way to a microbial ecological network in the gut. Thus, the capacity of A. muciniphila to utilize human milk will enable its survival in the early life intestine and colonization of the mucosal layer in early life, warranting later life mucosal and metabolic health.

SUBMITTER: Kostopoulos I

PROVIDER: S-EPMC7459334 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Akkermansia muciniphila uses human milk oligosaccharides to thrive in the early life conditions in vitro.

Kostopoulos Ioannis I Elzinga Janneke J Ottman Noora N Klievink Jay T JT Blijenberg Bernadet B Aalvink Steven S Boeren Sjef S Mank Marko M Knol Jan J de Vos Willem M WM Belzer Clara C

Scientific reports 20200831 1

Akkermansia muciniphila is a well-studied anaerobic bacterium specialized in mucus degradation and associated with human health. Because of the structural resemblance of mucus glycans and free human milk oligosaccharides (HMOs), we studied the ability of A. muciniphila to utilize human milk oligosaccharides. We found that A. muciniphila was able to grow on human milk and degrade HMOs. Analyses of the proteome of A. muciniphila indicated that key-glycan degrading enzymes were expressed when the b ...[more]

PMID: 32868839

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Project description:Akkermansia muciniphila is considered a next-generation probiotic because of its immense potential to regulate disorders. We isolated 31 strains of A. muciniphila from feces or breast milk of healthy people. After genome sequencing, assembly, and analysis, we selected six strains (AM01 to AM06) for further exploration. We first analyzed their general characteristics, including morphological description, growth characteristics, and physiological and biochemical characteristics, and then confirmed their genetic characteristics, including GC content, putative virulence factors, and antibiotic resistance genes. We next investigated the tolerance of these strains to artificial gastric and intestinal fluids and bile salts to evaluate their survival potential in the digestive tract. Drug sensitivity tests were also conducted based on the analysis of the antibiotic resistance genes of these strains. Furthermore, we examined the genetic stability and acute toxicity of two strains (AM02 and AM06) in mice. Finally, the safety of AM06 was evaluated in normal mice and nude mice. AM06 exhibited adaptability to pH changes. Since AM02 and AM03 showed more resistance to antibiotics than AM01 and AM04 to AM06, their potential clinical application may be limited. Both AM02 and AM06 were genetically and phenotypically stable and safe in normal mice, and AM06 was safe in nude mice. Considering all this together, AM06 is a safe A. muciniphila strain and exhibits a great potential for use as a probiotic strain among the isolated strains. IMPORTANCE In this study, we isolated 30 strains of Akkermansia muciniphila from different samples of human feces, and for the first time we isolated an A. muciniphila strain from human breast milk. This isolation verified the existence of microbes in human breast milk, which suggests that A. muciniphila can be vertically propagated from mother to infant and participates in the formation of the early gut microbiome. We then systematically evaluated the potential for use as a probiotic of this A. muciniphila strains according to the FAO/WHO recommendation. We confirmed that the AM06 strain isolated from breast milk has no virulence factors and is genetically stable and nonpathogenic for both normal mice and nude mice. Moreover, its tolerance to pH changes and bile salts indicates its desirable probiotic properties. Thus, we propose that the AM06 strain of A. muciniphila is safe for use as a probiotic candidate.

Project description: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. IMPORTANCE Human milk oligosaccharides (HMOs) are the third most abundant component of breast milk and provide several benefits to developing infants, including the recruitment of beneficial bacteria to the human gut. Akkermansia strains are largely considered beneficial bacteria and have been detected in colostrum, breast milk, and young infants. A. muciniphila MucT, belonging to the AmI phylogroup, contributes to the HMO deconstruction capacity of the infant. Here, using phylogenomics, we examined the genomic capacities of four Akkermansia phylogroups to deconstruct HMOs. Indeed, each phylogroup contained differences in their genomic capacities to deconstruct HMOs, and representative strains of each phylogroup were able to grow using HMOs. These Akkermansia-HMO interactions potentially influence gut microbial ecology in early life, a critical time for the development of the gut microbiome and infant health.

Dataset Information

Akkermansia muciniphila uses human milk oligosaccharides to thrive in the early life conditions in vitro.

Publications

Akkermansia muciniphila uses human milk oligosaccharides to thrive in the early life conditions in vitro.

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