Strain-Level Analysis of <italic toggle="yes">Bifidobacterium</italic> spp. from Gut Microbiomes of Adults with Differing Lactase Persistence Genotypes

ABSTRACT One of the strongest associations between human genetics and the gut microbiome is a greater relative abundance of Bifidobacterium in adults with lactase gene (LCT) single nucleotide polymorphisms (SNPs) associated with lactase nonpersistence (GG genotypes), versus lactase persistence (AA/A...

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Autores principales:	Victor Schmidt, Hagay Enav, Timothy D. Spector, Nicholas D. Youngblut, Ruth E. Ley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Bifidobacterium lactase persistence microbiome strain stability gut microbiome human microbiome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ce9e9996ef3b4657835d64928208c8ee
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spelling	oai:doaj.org-article:ce9e9996ef3b4657835d64928208c8ee2021-12-02T18:15:46ZStrain-Level Analysis of <italic toggle="yes">Bifidobacterium</italic> spp. from Gut Microbiomes of Adults with Differing Lactase Persistence Genotypes10.1128/mSystems.00911-202379-5077https://doaj.org/article/ce9e9996ef3b4657835d64928208c8ee2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00911-20https://doaj.org/toc/2379-5077ABSTRACT One of the strongest associations between human genetics and the gut microbiome is a greater relative abundance of Bifidobacterium in adults with lactase gene (LCT) single nucleotide polymorphisms (SNPs) associated with lactase nonpersistence (GG genotypes), versus lactase persistence (AA/AG genotypes). To gain a finer-grained phylogenetic resolution of this association, we interrogated 1,680 16S rRNA libraries and 245 metagenomes from gut microbiomes of adults with various lactase persistence genotypes. We further employed a novel genome-capture-based enrichment of Bifidobacterium DNA from a subset of these metagenomes, including monozygotic (MZ) twin pairs, each sampled 2 or 3 times. B. adolescentis and B. longum were the most abundant Bifidobacterium species regardless of host LCT genotype. LCT genotypes could not be discriminated based on relative abundances of Bifidobacterium species or Bifidobacterium community structure. Three distinct metagenomic analysis methods of Bifidobacterium-enriched DNA revealed intraindividual temporal stability of B. longum, B. adolescentis, and B. bifidum strains against the background of a changeable microbiome. Two of our three methods also observed greater strain sharing within MZ twin pairs than within unrelated individuals for B. adolescentis, while no method revealed an effect of host LCT genotype on Bifidobacterium strain composition. Our results support a “rising tide lifts all boats” model for the dominant bifidobacteria in the adult gut: their higher abundance in lactase-nonpersistent than in lactase-persistent individuals results from an expansion at the genus level. Bifidobacterium species are known to be transmitted from mother to child and stable within individuals in infancy and childhood: our results extend this stability into adulthood. IMPORTANCE When humans domesticated animals, some adapted genetically to digest milk into adulthood (lactase persistence). The gut microbiomes of people with lactase-persistent genotypes (AA or AG) differ from those with lactase-nonpersistent genotypes (GG) by containing fewer bacteria belonging to the bifidobacteria, a group which contains beneficial species. Here, we asked if the gut microbiomes of adults with GG and AA/AG genotypes differ in the species of bifidobacteria present. In particular, we used a novel technique which allowed us to compare bifidobacteria in adults at the strain level, without the traditional need for culturing. Our results show that the GG genotype enhances the abundance of bifidobacteria regardless of species. We also noted that a person’s specific strains are recoverable several years later, and twins can share the same ones. Given that bifidobacteria are inherited from mother to child, strain stability over time in adulthood suggests long-term, multigenerational inheritance.Victor SchmidtHagay EnavTimothy D. SpectorNicholas D. YoungblutRuth E. LeyAmerican Society for MicrobiologyarticleBifidobacteriumlactase persistencemicrobiomestrain stabilitygut microbiomehuman microbiomeMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bifidobacterium lactase persistence microbiome strain stability gut microbiome human microbiome Microbiology QR1-502
spellingShingle	Bifidobacterium lactase persistence microbiome strain stability gut microbiome human microbiome Microbiology QR1-502 Victor Schmidt Hagay Enav Timothy D. Spector Nicholas D. Youngblut Ruth E. Ley Strain-Level Analysis of <italic toggle="yes">Bifidobacterium</italic> spp. from Gut Microbiomes of Adults with Differing Lactase Persistence Genotypes
description	ABSTRACT One of the strongest associations between human genetics and the gut microbiome is a greater relative abundance of Bifidobacterium in adults with lactase gene (LCT) single nucleotide polymorphisms (SNPs) associated with lactase nonpersistence (GG genotypes), versus lactase persistence (AA/AG genotypes). To gain a finer-grained phylogenetic resolution of this association, we interrogated 1,680 16S rRNA libraries and 245 metagenomes from gut microbiomes of adults with various lactase persistence genotypes. We further employed a novel genome-capture-based enrichment of Bifidobacterium DNA from a subset of these metagenomes, including monozygotic (MZ) twin pairs, each sampled 2 or 3 times. B. adolescentis and B. longum were the most abundant Bifidobacterium species regardless of host LCT genotype. LCT genotypes could not be discriminated based on relative abundances of Bifidobacterium species or Bifidobacterium community structure. Three distinct metagenomic analysis methods of Bifidobacterium-enriched DNA revealed intraindividual temporal stability of B. longum, B. adolescentis, and B. bifidum strains against the background of a changeable microbiome. Two of our three methods also observed greater strain sharing within MZ twin pairs than within unrelated individuals for B. adolescentis, while no method revealed an effect of host LCT genotype on Bifidobacterium strain composition. Our results support a “rising tide lifts all boats” model for the dominant bifidobacteria in the adult gut: their higher abundance in lactase-nonpersistent than in lactase-persistent individuals results from an expansion at the genus level. Bifidobacterium species are known to be transmitted from mother to child and stable within individuals in infancy and childhood: our results extend this stability into adulthood. IMPORTANCE When humans domesticated animals, some adapted genetically to digest milk into adulthood (lactase persistence). The gut microbiomes of people with lactase-persistent genotypes (AA or AG) differ from those with lactase-nonpersistent genotypes (GG) by containing fewer bacteria belonging to the bifidobacteria, a group which contains beneficial species. Here, we asked if the gut microbiomes of adults with GG and AA/AG genotypes differ in the species of bifidobacteria present. In particular, we used a novel technique which allowed us to compare bifidobacteria in adults at the strain level, without the traditional need for culturing. Our results show that the GG genotype enhances the abundance of bifidobacteria regardless of species. We also noted that a person’s specific strains are recoverable several years later, and twins can share the same ones. Given that bifidobacteria are inherited from mother to child, strain stability over time in adulthood suggests long-term, multigenerational inheritance.
format	article
author	Victor Schmidt Hagay Enav Timothy D. Spector Nicholas D. Youngblut Ruth E. Ley
author_facet	Victor Schmidt Hagay Enav Timothy D. Spector Nicholas D. Youngblut Ruth E. Ley
author_sort	Victor Schmidt
title	Strain-Level Analysis of <italic toggle="yes">Bifidobacterium</italic> spp. from Gut Microbiomes of Adults with Differing Lactase Persistence Genotypes
title_short	Strain-Level Analysis of <italic toggle="yes">Bifidobacterium</italic> spp. from Gut Microbiomes of Adults with Differing Lactase Persistence Genotypes
title_full	Strain-Level Analysis of <italic toggle="yes">Bifidobacterium</italic> spp. from Gut Microbiomes of Adults with Differing Lactase Persistence Genotypes
title_fullStr	Strain-Level Analysis of <italic toggle="yes">Bifidobacterium</italic> spp. from Gut Microbiomes of Adults with Differing Lactase Persistence Genotypes
title_full_unstemmed	Strain-Level Analysis of <italic toggle="yes">Bifidobacterium</italic> spp. from Gut Microbiomes of Adults with Differing Lactase Persistence Genotypes
title_sort	strain-level analysis of <italic toggle="yes">bifidobacterium</italic> spp. from gut microbiomes of adults with differing lactase persistence genotypes
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/ce9e9996ef3b4657835d64928208c8ee
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Strain-Level Analysis of <italic toggle="yes">Bifidobacterium</italic> spp. from Gut Microbiomes of Adults with Differing Lactase Persistence Genotypes

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