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Butyrate Levels in the Transition from an Infant- to an Adult-Like Gut Microbiota Correlate with Bacterial Networks Associated with Eubacterium Rectale and Ruminococcus Gnavus

Relatively little is known about the ecological forces shaping the gut microbiota composition during infancy. Therefore, the objective of the present study was to identify the nutrient utilization- and short-chain fatty acid (SCFA) production potential of gut microbes in infants during the first yea...

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Autores principales: Nilsen, Morten, Madelen Saunders, Carina, Leena Angell, Inga, Arntzen, Magnus Ø., Lødrup Carlsen, Karin C., Carlsen, Kai-Håkon, Haugen, Guttorm, Heldal Hagen, Live, Carlsen, Monica H., Hedlin, Gunilla, Monceyron Jonassen, Christine, Nordlund, Björn, Maria Rehbinder, Eva, Skjerven, Håvard O., Snipen, Lars, Cathrine Staff, Anne, Vettukattil, Riyas, Rudi, Knut
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7690385/
https://www.ncbi.nlm.nih.gov/pubmed/33105702
http://dx.doi.org/10.3390/genes11111245
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author Nilsen, Morten
Madelen Saunders, Carina
Leena Angell, Inga
Arntzen, Magnus Ø.
Lødrup Carlsen, Karin C.
Carlsen, Kai-Håkon
Haugen, Guttorm
Heldal Hagen, Live
Carlsen, Monica H.
Hedlin, Gunilla
Monceyron Jonassen, Christine
Nordlund, Björn
Maria Rehbinder, Eva
Skjerven, Håvard O.
Snipen, Lars
Cathrine Staff, Anne
Vettukattil, Riyas
Rudi, Knut
author_facet Nilsen, Morten
Madelen Saunders, Carina
Leena Angell, Inga
Arntzen, Magnus Ø.
Lødrup Carlsen, Karin C.
Carlsen, Kai-Håkon
Haugen, Guttorm
Heldal Hagen, Live
Carlsen, Monica H.
Hedlin, Gunilla
Monceyron Jonassen, Christine
Nordlund, Björn
Maria Rehbinder, Eva
Skjerven, Håvard O.
Snipen, Lars
Cathrine Staff, Anne
Vettukattil, Riyas
Rudi, Knut
author_sort Nilsen, Morten
collection PubMed
description Relatively little is known about the ecological forces shaping the gut microbiota composition during infancy. Therefore, the objective of the present study was to identify the nutrient utilization- and short-chain fatty acid (SCFA) production potential of gut microbes in infants during the first year of life. Stool samples were obtained from mothers at 18 weeks of pregnancy and from infants at birth (first stool) at 3, 6, and 12-months of age from the general population-based PreventADALL cohort. We identified the taxonomic and SCFA composition in 100 mother-child pairs. The SCFA production and substrate utilization potential of gut microbes were observed by multiomics (shotgun sequencing and proteomics) on six infants. We found a four-fold increase in relative butyrate levels from 6 to 12 months of infant age. The increase was correlated to Eubacterium rectale and its bacterial network, and Faecalibacterium prausnitzii relative abundance, while low butyrate at 12 months was correlated to Ruminococcus gnavus and its associated network of bacteria. Both E. rectale and F. prausnitzii expressed enzymes needed for butyrate production and enzymes related to dietary fiber degradation, while R. gnavus expressed mucus-, fucose, and human milk oligosaccharides (HMO)-related degradation enzymes. Therefore, we believe that the presence of E. rectale, its network, and F. prausnitzii are key bacteria in the transition from an infant- to an adult-like gut microbiota with respect to butyrate production. Our results indicate that the transition from an infant- to an adult-like gut microbiota with respect to butyrate producing bacteria, occurs between 6 and 12 months of infant age. The bacteria associated with the increased butyrate ratio/levels were E. rectale and F. prausnitzii, which potentially utilize a variety of dietary fibers based on the glycoside hydrolases (GHs) expressed. R. gnavus with a negative association to butyrate potentially utilizes mucin, fucose, and HMO components. This knowledge could have future importance in understanding how microbial metabolites can impact infant health and development.
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spelling pubmed-76903852020-11-27 Butyrate Levels in the Transition from an Infant- to an Adult-Like Gut Microbiota Correlate with Bacterial Networks Associated with Eubacterium Rectale and Ruminococcus Gnavus Nilsen, Morten Madelen Saunders, Carina Leena Angell, Inga Arntzen, Magnus Ø. Lødrup Carlsen, Karin C. Carlsen, Kai-Håkon Haugen, Guttorm Heldal Hagen, Live Carlsen, Monica H. Hedlin, Gunilla Monceyron Jonassen, Christine Nordlund, Björn Maria Rehbinder, Eva Skjerven, Håvard O. Snipen, Lars Cathrine Staff, Anne Vettukattil, Riyas Rudi, Knut Genes (Basel) Article Relatively little is known about the ecological forces shaping the gut microbiota composition during infancy. Therefore, the objective of the present study was to identify the nutrient utilization- and short-chain fatty acid (SCFA) production potential of gut microbes in infants during the first year of life. Stool samples were obtained from mothers at 18 weeks of pregnancy and from infants at birth (first stool) at 3, 6, and 12-months of age from the general population-based PreventADALL cohort. We identified the taxonomic and SCFA composition in 100 mother-child pairs. The SCFA production and substrate utilization potential of gut microbes were observed by multiomics (shotgun sequencing and proteomics) on six infants. We found a four-fold increase in relative butyrate levels from 6 to 12 months of infant age. The increase was correlated to Eubacterium rectale and its bacterial network, and Faecalibacterium prausnitzii relative abundance, while low butyrate at 12 months was correlated to Ruminococcus gnavus and its associated network of bacteria. Both E. rectale and F. prausnitzii expressed enzymes needed for butyrate production and enzymes related to dietary fiber degradation, while R. gnavus expressed mucus-, fucose, and human milk oligosaccharides (HMO)-related degradation enzymes. Therefore, we believe that the presence of E. rectale, its network, and F. prausnitzii are key bacteria in the transition from an infant- to an adult-like gut microbiota with respect to butyrate production. Our results indicate that the transition from an infant- to an adult-like gut microbiota with respect to butyrate producing bacteria, occurs between 6 and 12 months of infant age. The bacteria associated with the increased butyrate ratio/levels were E. rectale and F. prausnitzii, which potentially utilize a variety of dietary fibers based on the glycoside hydrolases (GHs) expressed. R. gnavus with a negative association to butyrate potentially utilizes mucin, fucose, and HMO components. This knowledge could have future importance in understanding how microbial metabolites can impact infant health and development. MDPI 2020-10-22 /pmc/articles/PMC7690385/ /pubmed/33105702 http://dx.doi.org/10.3390/genes11111245 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Nilsen, Morten
Madelen Saunders, Carina
Leena Angell, Inga
Arntzen, Magnus Ø.
Lødrup Carlsen, Karin C.
Carlsen, Kai-Håkon
Haugen, Guttorm
Heldal Hagen, Live
Carlsen, Monica H.
Hedlin, Gunilla
Monceyron Jonassen, Christine
Nordlund, Björn
Maria Rehbinder, Eva
Skjerven, Håvard O.
Snipen, Lars
Cathrine Staff, Anne
Vettukattil, Riyas
Rudi, Knut
Butyrate Levels in the Transition from an Infant- to an Adult-Like Gut Microbiota Correlate with Bacterial Networks Associated with Eubacterium Rectale and Ruminococcus Gnavus
title Butyrate Levels in the Transition from an Infant- to an Adult-Like Gut Microbiota Correlate with Bacterial Networks Associated with Eubacterium Rectale and Ruminococcus Gnavus
title_full Butyrate Levels in the Transition from an Infant- to an Adult-Like Gut Microbiota Correlate with Bacterial Networks Associated with Eubacterium Rectale and Ruminococcus Gnavus
title_fullStr Butyrate Levels in the Transition from an Infant- to an Adult-Like Gut Microbiota Correlate with Bacterial Networks Associated with Eubacterium Rectale and Ruminococcus Gnavus
title_full_unstemmed Butyrate Levels in the Transition from an Infant- to an Adult-Like Gut Microbiota Correlate with Bacterial Networks Associated with Eubacterium Rectale and Ruminococcus Gnavus
title_short Butyrate Levels in the Transition from an Infant- to an Adult-Like Gut Microbiota Correlate with Bacterial Networks Associated with Eubacterium Rectale and Ruminococcus Gnavus
title_sort butyrate levels in the transition from an infant- to an adult-like gut microbiota correlate with bacterial networks associated with eubacterium rectale and ruminococcus gnavus
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7690385/
https://www.ncbi.nlm.nih.gov/pubmed/33105702
http://dx.doi.org/10.3390/genes11111245
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