Syntrophy via Interspecies H<sub>2</sub> Transfer between <italic toggle="yes">Christensenella</italic> and <italic toggle="yes">Methanobrevibacter</italic> Underlies Their Global Cooccurrence in the Human Gut

ABSTRACT Across human populations, 16S rRNA gene-based surveys of gut microbiomes have revealed that the bacterial family Christensenellaceae and the archaeal family Methanobacteriaceae cooccur and are enriched in individuals with a lean, compared to an obese, body mass index (BMI). Whether these as...

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Autores principales:	Albane Ruaud, Sofia Esquivel-Elizondo, Jacobo de la Cuesta-Zuluaga, Jillian L. Waters, Largus T. Angenent, Nicholas D. Youngblut, Ruth E. Ley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	human gut methanogens microbiome syntrophy Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/10050acb3b7c450a86f32d4d3056a83c
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spelling	oai:doaj.org-article:10050acb3b7c450a86f32d4d3056a83c2021-11-15T15:56:57ZSyntrophy via Interspecies H<sub>2</sub> Transfer between <italic toggle="yes">Christensenella</italic> and <italic toggle="yes">Methanobrevibacter</italic> Underlies Their Global Cooccurrence in the Human Gut10.1128/mBio.03235-192150-7511https://doaj.org/article/10050acb3b7c450a86f32d4d3056a83c2020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.03235-19https://doaj.org/toc/2150-7511ABSTRACT Across human populations, 16S rRNA gene-based surveys of gut microbiomes have revealed that the bacterial family Christensenellaceae and the archaeal family Methanobacteriaceae cooccur and are enriched in individuals with a lean, compared to an obese, body mass index (BMI). Whether these association patterns reflect interactions between metabolic partners, as well as whether these associations play a role in the lean host phenotype with which they associate, remains to be ascertained. Here, we validated previously reported cooccurrence patterns of the two families and their association with a lean BMI with a meta-analysis of 1,821 metagenomes derived from 10 independent studies. Furthermore, we report positive associations at the genus and species levels between Christensenella spp. and Methanobrevibacter smithii, the most abundant methanogen of the human gut. By coculturing three Christensenella spp. with M. smithii, we show that Christensenella spp. efficiently support the metabolism of M. smithii via H2 production far better than Bacteroides thetaiotaomicron does. Christensenella minuta forms flocs colonized by M. smithii even when H2 is in excess. In culture with C. minuta, H2 consumption by M. smithii shifts the metabolic output of C. minuta’s fermentation toward acetate rather than butyrate. Together, these results indicate that the widespread cooccurrence of these microorganisms is underpinned by both physical and metabolic interactions. Their combined metabolic activity may provide insights into their association with a lean host BMI. IMPORTANCE The human gut microbiome is made of trillions of microbial cells, most of which are Bacteria, with a subset of Archaea. The bacterial family Christensenellaceae and the archaeal family Methanobacteriaceae are widespread in human guts. They correlate with each other and with a lean body type. Whether species of these two families interact and how they affect the body type are unanswered questions. Here, we show that species within these families correlate with each other across people. We also demonstrate that particular species of these two families grow together in dense flocs, wherein the bacteria provide hydrogen gas to the archaea, which then make methane. When the archaea are present, the ratio of bacterial products (which are nutrients for humans) is changed. These observations indicate that when these species grow together, their products have the potential to affect the physiology of their human host.Albane RuaudSofia Esquivel-ElizondoJacobo de la Cuesta-ZuluagaJillian L. WatersLargus T. AngenentNicholas D. YoungblutRuth E. LeyAmerican Society for Microbiologyarticlehuman gutmethanogensmicrobiomesyntrophyMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	human gut methanogens microbiome syntrophy Microbiology QR1-502
spellingShingle	human gut methanogens microbiome syntrophy Microbiology QR1-502 Albane Ruaud Sofia Esquivel-Elizondo Jacobo de la Cuesta-Zuluaga Jillian L. Waters Largus T. Angenent Nicholas D. Youngblut Ruth E. Ley Syntrophy via Interspecies H<sub>2</sub> Transfer between <italic toggle="yes">Christensenella</italic> and <italic toggle="yes">Methanobrevibacter</italic> Underlies Their Global Cooccurrence in the Human Gut
description	ABSTRACT Across human populations, 16S rRNA gene-based surveys of gut microbiomes have revealed that the bacterial family Christensenellaceae and the archaeal family Methanobacteriaceae cooccur and are enriched in individuals with a lean, compared to an obese, body mass index (BMI). Whether these association patterns reflect interactions between metabolic partners, as well as whether these associations play a role in the lean host phenotype with which they associate, remains to be ascertained. Here, we validated previously reported cooccurrence patterns of the two families and their association with a lean BMI with a meta-analysis of 1,821 metagenomes derived from 10 independent studies. Furthermore, we report positive associations at the genus and species levels between Christensenella spp. and Methanobrevibacter smithii, the most abundant methanogen of the human gut. By coculturing three Christensenella spp. with M. smithii, we show that Christensenella spp. efficiently support the metabolism of M. smithii via H2 production far better than Bacteroides thetaiotaomicron does. Christensenella minuta forms flocs colonized by M. smithii even when H2 is in excess. In culture with C. minuta, H2 consumption by M. smithii shifts the metabolic output of C. minuta’s fermentation toward acetate rather than butyrate. Together, these results indicate that the widespread cooccurrence of these microorganisms is underpinned by both physical and metabolic interactions. Their combined metabolic activity may provide insights into their association with a lean host BMI. IMPORTANCE The human gut microbiome is made of trillions of microbial cells, most of which are Bacteria, with a subset of Archaea. The bacterial family Christensenellaceae and the archaeal family Methanobacteriaceae are widespread in human guts. They correlate with each other and with a lean body type. Whether species of these two families interact and how they affect the body type are unanswered questions. Here, we show that species within these families correlate with each other across people. We also demonstrate that particular species of these two families grow together in dense flocs, wherein the bacteria provide hydrogen gas to the archaea, which then make methane. When the archaea are present, the ratio of bacterial products (which are nutrients for humans) is changed. These observations indicate that when these species grow together, their products have the potential to affect the physiology of their human host.
format	article
author	Albane Ruaud Sofia Esquivel-Elizondo Jacobo de la Cuesta-Zuluaga Jillian L. Waters Largus T. Angenent Nicholas D. Youngblut Ruth E. Ley
author_facet	Albane Ruaud Sofia Esquivel-Elizondo Jacobo de la Cuesta-Zuluaga Jillian L. Waters Largus T. Angenent Nicholas D. Youngblut Ruth E. Ley
author_sort	Albane Ruaud
title	Syntrophy via Interspecies H<sub>2</sub> Transfer between <italic toggle="yes">Christensenella</italic> and <italic toggle="yes">Methanobrevibacter</italic> Underlies Their Global Cooccurrence in the Human Gut
title_short	Syntrophy via Interspecies H<sub>2</sub> Transfer between <italic toggle="yes">Christensenella</italic> and <italic toggle="yes">Methanobrevibacter</italic> Underlies Their Global Cooccurrence in the Human Gut
title_full	Syntrophy via Interspecies H<sub>2</sub> Transfer between <italic toggle="yes">Christensenella</italic> and <italic toggle="yes">Methanobrevibacter</italic> Underlies Their Global Cooccurrence in the Human Gut
title_fullStr	Syntrophy via Interspecies H<sub>2</sub> Transfer between <italic toggle="yes">Christensenella</italic> and <italic toggle="yes">Methanobrevibacter</italic> Underlies Their Global Cooccurrence in the Human Gut
title_full_unstemmed	Syntrophy via Interspecies H<sub>2</sub> Transfer between <italic toggle="yes">Christensenella</italic> and <italic toggle="yes">Methanobrevibacter</italic> Underlies Their Global Cooccurrence in the Human Gut
title_sort	syntrophy via interspecies h<sub>2</sub> transfer between <italic toggle="yes">christensenella</italic> and <italic toggle="yes">methanobrevibacter</italic> underlies their global cooccurrence in the human gut
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/10050acb3b7c450a86f32d4d3056a83c
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Syntrophy via Interspecies H<sub>2</sub> Transfer between <italic toggle="yes">Christensenella</italic> and <italic toggle="yes">Methanobrevibacter</italic> Underlies Their Global Cooccurrence in the Human Gut

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