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Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort

BACKGROUND: The gut is the most extensively studied niche of the human microbiome. The aim of this study was to characterise the initial gut microbiota development of a cohort of breastfed infants (n = 192) from 1 to 24 weeks of age. METHODS: V4-V5 region 16S rRNA amplicon Illumina sequencing and,...

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Autores principales: Hill, Cian J., Lynch, Denise B., Murphy, Kiera, Ulaszewska, Marynka, Jeffery, Ian B., O’Shea, Carol Anne, Watkins, Claire, Dempsey, Eugene, Mattivi, Fulvio, Touhy, Kieran, Ross, R. Paul, Ryan, C. Anthony, O’ Toole, Paul W., Stanton, Catherine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5240274/
https://www.ncbi.nlm.nih.gov/pubmed/28095889
http://dx.doi.org/10.1186/s40168-016-0213-y
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author Hill, Cian J.
Lynch, Denise B.
Murphy, Kiera
Ulaszewska, Marynka
Jeffery, Ian B.
O’Shea, Carol Anne
Watkins, Claire
Dempsey, Eugene
Mattivi, Fulvio
Touhy, Kieran
Ross, R. Paul
Ryan, C. Anthony
O’ Toole, Paul W.
Stanton, Catherine
author_facet Hill, Cian J.
Lynch, Denise B.
Murphy, Kiera
Ulaszewska, Marynka
Jeffery, Ian B.
O’Shea, Carol Anne
Watkins, Claire
Dempsey, Eugene
Mattivi, Fulvio
Touhy, Kieran
Ross, R. Paul
Ryan, C. Anthony
O’ Toole, Paul W.
Stanton, Catherine
author_sort Hill, Cian J.
collection PubMed
description BACKGROUND: The gut is the most extensively studied niche of the human microbiome. The aim of this study was to characterise the initial gut microbiota development of a cohort of breastfed infants (n = 192) from 1 to 24 weeks of age. METHODS: V4-V5 region 16S rRNA amplicon Illumina sequencing and, in parallel, bacteriological culture. The metabolomic profile of infant urine at 4 weeks of age was also examined by LC-MS. RESULTS: Full-term (FT), spontaneous vaginally delivered (SVD) infants’ microbiota remained stable at both phylum and genus levels during the 24-week period examined. FT Caesarean section (CS) infants displayed an increased faecal abundance of Firmicutes (p < 0.01) and lower abundance of Actinobacteria (p < 0.001) after the first week of life compared to FT-SVD infants. FT-CS infants gradually progressed to harbouring a microbiota closely resembling FT-SVD (which remained stable) by week 8 of life, which was maintained at week 24. The gut microbiota of preterm (PT) infants displayed a significantly greater abundance of Proteobacteria compared to FT infants (p < 0.001) at week 1. Metabolomic analysis of urine at week 4 indicated PT-CS infants have a functionally different metabolite profile than FT (both CS and SVD) infants. Co-inertia analysis showed co-variation between the urine metabolome and the faecal microbiota of the infants. Tryptophan and tyrosine metabolic pathways, as well as fatty acid and bile acid metabolism, were found to be affected by delivery mode and gestational age. CONCLUSIONS: These findings confirm that mode of delivery and gestational age both have significant effects on early neonatal microbiota composition. There is also a significant difference between the metabolite profile of FT and PT infants. Prolonged breastfeeding was shown to have a significant effect on the microbiota composition of FT-CS infants at 24 weeks of age, but interestingly not on that of FT-SVD infants. Twins had more similar microbiota to one another than between two random infants, reflecting the influence of similarities in both host genetics and the environment on the microbiota. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40168-016-0213-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-52402742017-01-19 Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort Hill, Cian J. Lynch, Denise B. Murphy, Kiera Ulaszewska, Marynka Jeffery, Ian B. O’Shea, Carol Anne Watkins, Claire Dempsey, Eugene Mattivi, Fulvio Touhy, Kieran Ross, R. Paul Ryan, C. Anthony O’ Toole, Paul W. Stanton, Catherine Microbiome Research BACKGROUND: The gut is the most extensively studied niche of the human microbiome. The aim of this study was to characterise the initial gut microbiota development of a cohort of breastfed infants (n = 192) from 1 to 24 weeks of age. METHODS: V4-V5 region 16S rRNA amplicon Illumina sequencing and, in parallel, bacteriological culture. The metabolomic profile of infant urine at 4 weeks of age was also examined by LC-MS. RESULTS: Full-term (FT), spontaneous vaginally delivered (SVD) infants’ microbiota remained stable at both phylum and genus levels during the 24-week period examined. FT Caesarean section (CS) infants displayed an increased faecal abundance of Firmicutes (p < 0.01) and lower abundance of Actinobacteria (p < 0.001) after the first week of life compared to FT-SVD infants. FT-CS infants gradually progressed to harbouring a microbiota closely resembling FT-SVD (which remained stable) by week 8 of life, which was maintained at week 24. The gut microbiota of preterm (PT) infants displayed a significantly greater abundance of Proteobacteria compared to FT infants (p < 0.001) at week 1. Metabolomic analysis of urine at week 4 indicated PT-CS infants have a functionally different metabolite profile than FT (both CS and SVD) infants. Co-inertia analysis showed co-variation between the urine metabolome and the faecal microbiota of the infants. Tryptophan and tyrosine metabolic pathways, as well as fatty acid and bile acid metabolism, were found to be affected by delivery mode and gestational age. CONCLUSIONS: These findings confirm that mode of delivery and gestational age both have significant effects on early neonatal microbiota composition. There is also a significant difference between the metabolite profile of FT and PT infants. Prolonged breastfeeding was shown to have a significant effect on the microbiota composition of FT-CS infants at 24 weeks of age, but interestingly not on that of FT-SVD infants. Twins had more similar microbiota to one another than between two random infants, reflecting the influence of similarities in both host genetics and the environment on the microbiota. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40168-016-0213-y) contains supplementary material, which is available to authorized users. BioMed Central 2017-01-17 /pmc/articles/PMC5240274/ /pubmed/28095889 http://dx.doi.org/10.1186/s40168-016-0213-y Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Hill, Cian J.
Lynch, Denise B.
Murphy, Kiera
Ulaszewska, Marynka
Jeffery, Ian B.
O’Shea, Carol Anne
Watkins, Claire
Dempsey, Eugene
Mattivi, Fulvio
Touhy, Kieran
Ross, R. Paul
Ryan, C. Anthony
O’ Toole, Paul W.
Stanton, Catherine
Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort
title Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort
title_full Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort
title_fullStr Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort
title_full_unstemmed Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort
title_short Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort
title_sort evolution of gut microbiota composition from birth to 24 weeks in the infantmet cohort
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5240274/
https://www.ncbi.nlm.nih.gov/pubmed/28095889
http://dx.doi.org/10.1186/s40168-016-0213-y
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