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

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 in the infant gut. Human milk oligosaccharides (HMOs) are abundant compon...

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Veröffentlicht in:Applied and environmental microbiology 2022-01, Vol.88 (1), p.e0148721-e0148721
Hauptverfasser: Luna, Estefani, Parkar, Shanthi G, Kirmiz, Nina, Hartel, Stephanie, Hearn, Erik, Hossine, Marziiah, Kurdian, Arinnae, Mendoza, Claudia, Orr, Katherine, Padilla, Loren, Ramirez, Katherine, Salcedo, Priscilla, Serrano, Erik, Choudhury, Biswa, Paulchakrabarti, Mousumi, Parker, Craig T, Huynh, Steven, Cooper, Kerry, Flores, Gilberto E
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container_issue 1
container_start_page e0148721
container_title Applied and environmental microbiology
container_volume 88
creator Luna, Estefani
Parkar, Shanthi G
Kirmiz, Nina
Hartel, Stephanie
Hearn, Erik
Hossine, Marziiah
Kurdian, Arinnae
Mendoza, Claudia
Orr, Katherine
Padilla, Loren
Ramirez, Katherine
Salcedo, Priscilla
Serrano, Erik
Choudhury, Biswa
Paulchakrabarti, Mousumi
Parker, Craig T
Huynh, Steven
Cooper, Kerry
Flores, Gilberto E
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 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 . 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 to grow on HMOs. First, we screened 85 genomes representing the four known 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 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 strains representing all known phylogroups. Further studies are required to examine how HMO ingestion influences gut microbial ecology in infants harboring different phylogroups. 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. strains are largely considered beneficial bacteria and have been detected in colostrum, breast milk, and young infants. A. muciniphila Muc , belonging to the AmI phylogroup, contributes to the HMO deconstruction capacity of the infant. Here, using phylogenomics, we examined the genomic capacities of four 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 -HMO interactions potentially influence gut microbial ecology in early life, a critical time for the development of the gut microbiome and infant health.
doi_str_mv 10.1128/AEM.01487-21
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However, despite being detected by as early as 1 month of age, little is known about the role of 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 . 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 to grow on HMOs. First, we screened 85 genomes representing the four known 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 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 strains representing all known phylogroups. Further studies are required to examine how HMO ingestion influences gut microbial ecology in infants harboring different phylogroups. 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. strains are largely considered beneficial bacteria and have been detected in colostrum, breast milk, and young infants. A. muciniphila Muc , belonging to the AmI phylogroup, contributes to the HMO deconstruction capacity of the infant. Here, using phylogenomics, we examined the genomic capacities of four 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. 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However, despite being detected by as early as 1 month of age, little is known about the role of 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 . 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 to grow on HMOs. First, we screened 85 genomes representing the four known 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 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 strains representing all known phylogroups. Further studies are required to examine how HMO ingestion influences gut microbial ecology in infants harboring different phylogroups. 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. strains are largely considered beneficial bacteria and have been detected in colostrum, breast milk, and young infants. A. muciniphila Muc , belonging to the AmI phylogroup, contributes to the HMO deconstruction capacity of the infant. Here, using phylogenomics, we examined the genomic capacities of four 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 -HMO interactions potentially influence gut microbial ecology in early life, a critical time for the development of the gut microbiome and infant health.</description><subject>Akkermansia</subject><subject>Applied and Industrial Microbiology</subject><subject>Babies</subject><subject>Bacteria</subject><subject>Breast milk</subject><subject>Breastfeeding &amp; lactation</subject><subject>Colostrum</subject><subject>Deconstruction</subject><subject>Digestive system</subject><subject>Ecological effects</subject><subject>Enzymatic activity</subject><subject>Female</subject><subject>Gastrointestinal Microbiome</subject><subject>Gastrointestinal tract</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Glycosidases</subject><subject>Glycoside hydrolase</subject><subject>Humans</subject><subject>Infant</subject><subject>Infants</subject><subject>Ingestion</subject><subject>Intestinal microflora</subject><subject>Metabolites</subject><subject>Microbial Ecology</subject><subject>Microbiomes</subject><subject>Microorganisms</subject><subject>Milk, Human</subject><subject>Mucin</subject><subject>Oligosaccharides</subject><subject>Probiotics</subject><subject>Strains 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Stephanie</au><au>Hearn, Erik</au><au>Hossine, Marziiah</au><au>Kurdian, Arinnae</au><au>Mendoza, Claudia</au><au>Orr, Katherine</au><au>Padilla, Loren</au><au>Ramirez, Katherine</au><au>Salcedo, Priscilla</au><au>Serrano, Erik</au><au>Choudhury, Biswa</au><au>Paulchakrabarti, Mousumi</au><au>Parker, Craig T</au><au>Huynh, Steven</au><au>Cooper, Kerry</au><au>Flores, Gilberto E</au><au>McBain, Andrew J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Utilization Efficiency of Human Milk Oligosaccharides by Human-Associated Akkermansia Is Strain Dependent</atitle><jtitle>Applied and environmental microbiology</jtitle><stitle>Appl Environ Microbiol</stitle><addtitle>Appl Environ Microbiol</addtitle><date>2022-01-11</date><risdate>2022</risdate><volume>88</volume><issue>1</issue><spage>e0148721</spage><epage>e0148721</epage><pages>e0148721-e0148721</pages><issn>0099-2240</issn><eissn>1098-5336</eissn><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 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 . 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 to grow on HMOs. First, we screened 85 genomes representing the four known 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 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 strains representing all known phylogroups. Further studies are required to examine how HMO ingestion influences gut microbial ecology in infants harboring different phylogroups. 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. strains are largely considered beneficial bacteria and have been detected in colostrum, breast milk, and young infants. A. muciniphila Muc , belonging to the AmI phylogroup, contributes to the HMO deconstruction capacity of the infant. Here, using phylogenomics, we examined the genomic capacities of four 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 -HMO interactions potentially influence gut microbial ecology in early life, a critical time for the development of the gut microbiome and infant health.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>34669436</pmid><doi>10.1128/AEM.01487-21</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-3338-611X</orcidid><orcidid>https://orcid.org/0000-0002-5737-7867</orcidid><oa>free_for_read</oa></addata></record>
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ispartof Applied and environmental microbiology, 2022-01, Vol.88 (1), p.e0148721-e0148721
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1098-5336
language eng
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source American Society for Microbiology; MEDLINE; PubMed Central; Alma/SFX Local Collection
subjects Akkermansia
Applied and Industrial Microbiology
Babies
Bacteria
Breast milk
Breastfeeding & lactation
Colostrum
Deconstruction
Digestive system
Ecological effects
Enzymatic activity
Female
Gastrointestinal Microbiome
Gastrointestinal tract
Genomes
Genomics
Glycosidases
Glycoside hydrolase
Humans
Infant
Infants
Ingestion
Intestinal microflora
Metabolites
Microbial Ecology
Microbiomes
Microorganisms
Milk, Human
Mucin
Oligosaccharides
Probiotics
Strains (organisms)
Substrates
Verrucomicrobia
title Utilization Efficiency of Human Milk Oligosaccharides by Human-Associated Akkermansia Is Strain Dependent
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