Gut microbiota develop towards an adult profile in a sex-specific manner during puberty

Abstract Accumulating evidence indicates that gut microbiota may regulate sex-hormone levels in the host, with effects on reproductive health. Very little is known about the development of intestinal microbiota during puberty in humans. To assess the connection between pubertal timing and fecal micr...

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Autores principales: Katri Korpela, Sampo Kallio, Anne Salonen, Matti Hero, Anna Kaarina Kukkonen, Päivi J. Miettinen, Erkki Savilahti, Ella Kohva, Laura Kariola, Maria Suutela, Annika Tarkkanen, Willem M. de Vos, Taneli Raivio, Mikael Kuitunen
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Publicado: Nature Portfolio 2021
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Acceso en línea:https://doaj.org/article/f74c3f7d26c64fde912232857c968be9
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spelling oai:doaj.org-article:f74c3f7d26c64fde912232857c968be92021-12-05T12:15:43ZGut microbiota develop towards an adult profile in a sex-specific manner during puberty10.1038/s41598-021-02375-z2045-2322https://doaj.org/article/f74c3f7d26c64fde912232857c968be92021-12-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-02375-zhttps://doaj.org/toc/2045-2322Abstract Accumulating evidence indicates that gut microbiota may regulate sex-hormone levels in the host, with effects on reproductive health. Very little is known about the development of intestinal microbiota during puberty in humans. To assess the connection between pubertal timing and fecal microbiota, and to assess how fecal microbiota develop during puberty in comparison with adult microbiota, we utilized a Finnish allergy-prevention-trial cohort (Flora). Data collected at 13-year follow-up were compared with adult data from a different Finnish cohort. Among the 13-year-old participants we collected questionnaire information, growth data from school-health-system records and fecal samples from 148 participants. Reference adult fecal samples were received from the Health and Early Life Microbiota (HELMi) cohort (n = 840). Fecal microbiota were analyzed using 16S rRNA gene amplicon sequencing; the data were correlated with pubertal timing and compared with data on adult microbiota. Probiotic intervention in the allergy-prevention-trial cohort was considered as a confounding factor only. The main outcome was composition of the microbiota in relation to pubertal timing (time to/from peak growth velocity) in both sexes separately, and similarity to adult microbiota. In girls, fecal microbiota became more adult-like with pubertal progression (p = 0.009). No such development was observed in boys (p = 0.9). Both sexes showed a trend towards increasing relative abundance of estrogen-metabolizing Clostridia and decreasing Bacteroidia with pubertal development, but this was statistically significant in girls only (p = 0.03). In girls, pubertal timing was associated positively with exposure to cephalosporins prior to the age of 10. Our data support the hypothesis that gut microbiota, particularly members of Ruminococcaceae, may affect pubertal timing, possibly via regulating host sex-hormone levels. Trial registration The registration number for the allergy-prevention-trial cohort: ClinicalTrials.gov, NCT00298337, registered 1 March 2006—Retrospectively registered, https://clinicaltrials.gov/show/NCT00298337 . The adult-comparison cohort (HELMi) is NCT03996304.Katri KorpelaSampo KallioAnne SalonenMatti HeroAnna Kaarina KukkonenPäivi J. MiettinenErkki SavilahtiElla KohvaLaura KariolaMaria SuutelaAnnika TarkkanenWillem M. de VosTaneli RaivioMikael KuitunenNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-10 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Katri Korpela
Sampo Kallio
Anne Salonen
Matti Hero
Anna Kaarina Kukkonen
Päivi J. Miettinen
Erkki Savilahti
Ella Kohva
Laura Kariola
Maria Suutela
Annika Tarkkanen
Willem M. de Vos
Taneli Raivio
Mikael Kuitunen
Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
description Abstract Accumulating evidence indicates that gut microbiota may regulate sex-hormone levels in the host, with effects on reproductive health. Very little is known about the development of intestinal microbiota during puberty in humans. To assess the connection between pubertal timing and fecal microbiota, and to assess how fecal microbiota develop during puberty in comparison with adult microbiota, we utilized a Finnish allergy-prevention-trial cohort (Flora). Data collected at 13-year follow-up were compared with adult data from a different Finnish cohort. Among the 13-year-old participants we collected questionnaire information, growth data from school-health-system records and fecal samples from 148 participants. Reference adult fecal samples were received from the Health and Early Life Microbiota (HELMi) cohort (n = 840). Fecal microbiota were analyzed using 16S rRNA gene amplicon sequencing; the data were correlated with pubertal timing and compared with data on adult microbiota. Probiotic intervention in the allergy-prevention-trial cohort was considered as a confounding factor only. The main outcome was composition of the microbiota in relation to pubertal timing (time to/from peak growth velocity) in both sexes separately, and similarity to adult microbiota. In girls, fecal microbiota became more adult-like with pubertal progression (p = 0.009). No such development was observed in boys (p = 0.9). Both sexes showed a trend towards increasing relative abundance of estrogen-metabolizing Clostridia and decreasing Bacteroidia with pubertal development, but this was statistically significant in girls only (p = 0.03). In girls, pubertal timing was associated positively with exposure to cephalosporins prior to the age of 10. Our data support the hypothesis that gut microbiota, particularly members of Ruminococcaceae, may affect pubertal timing, possibly via regulating host sex-hormone levels. Trial registration The registration number for the allergy-prevention-trial cohort: ClinicalTrials.gov, NCT00298337, registered 1 March 2006—Retrospectively registered, https://clinicaltrials.gov/show/NCT00298337 . The adult-comparison cohort (HELMi) is NCT03996304.
format article
author Katri Korpela
Sampo Kallio
Anne Salonen
Matti Hero
Anna Kaarina Kukkonen
Päivi J. Miettinen
Erkki Savilahti
Ella Kohva
Laura Kariola
Maria Suutela
Annika Tarkkanen
Willem M. de Vos
Taneli Raivio
Mikael Kuitunen
author_facet Katri Korpela
Sampo Kallio
Anne Salonen
Matti Hero
Anna Kaarina Kukkonen
Päivi J. Miettinen
Erkki Savilahti
Ella Kohva
Laura Kariola
Maria Suutela
Annika Tarkkanen
Willem M. de Vos
Taneli Raivio
Mikael Kuitunen
author_sort Katri Korpela
title Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title_short Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title_full Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title_fullStr Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title_full_unstemmed Gut microbiota develop towards an adult profile in a sex-specific manner during puberty
title_sort gut microbiota develop towards an adult profile in a sex-specific manner during puberty
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/f74c3f7d26c64fde912232857c968be9
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