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Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women

Recent studies suggest that exercise alters the gut microbiome. We determined whether six-weeks endurance exercise, without changing diet, affected the gut metagenome and systemic metabolites of overweight women. Previously sedentary overweight women (n = 19) underwent a six-weeks endurance exercise...

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Autores principales: Munukka, Eveliina, Ahtiainen, Juha P., Puigbó, Pere, Jalkanen, Sirpa, Pahkala, Katja, Keskitalo, Anniina, Kujala, Urho M., Pietilä, Sami, Hollmén, Maija, Elo, Laura, Huovinen, Pentti, D'Auria, Giuseppe, Pekkala, Satu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6178902/
https://www.ncbi.nlm.nih.gov/pubmed/30337914
http://dx.doi.org/10.3389/fmicb.2018.02323
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author Munukka, Eveliina
Ahtiainen, Juha P.
Puigbó, Pere
Jalkanen, Sirpa
Pahkala, Katja
Keskitalo, Anniina
Kujala, Urho M.
Pietilä, Sami
Hollmén, Maija
Elo, Laura
Huovinen, Pentti
D'Auria, Giuseppe
Pekkala, Satu
author_facet Munukka, Eveliina
Ahtiainen, Juha P.
Puigbó, Pere
Jalkanen, Sirpa
Pahkala, Katja
Keskitalo, Anniina
Kujala, Urho M.
Pietilä, Sami
Hollmén, Maija
Elo, Laura
Huovinen, Pentti
D'Auria, Giuseppe
Pekkala, Satu
author_sort Munukka, Eveliina
collection PubMed
description Recent studies suggest that exercise alters the gut microbiome. We determined whether six-weeks endurance exercise, without changing diet, affected the gut metagenome and systemic metabolites of overweight women. Previously sedentary overweight women (n = 19) underwent a six-weeks endurance exercise intervention, but two were excluded due to antibiotic therapy. The gut microbiota composition and functions were analyzed by 16S rRNA gene amplicon sequencing and metagenomics. Body composition was analyzed with DXA X-ray densitometer and serum metabolomics with NMR metabolomics. Total energy and energy-yielding nutrient intakes were analyzed from food records using Micro-Nutrica software. Serum clinical variables were determined with KONELAB instrument. Soluble Vascular Adhesion Protein 1 (VAP-1) was measured with ELISA and its' enzymatic activity as produced hydrogen peroxide. The exercise intervention was effective, as maximal power and maximum rate of oxygen consumption increased while android fat mass decreased. No changes in diet were observed. Metagenomic analysis revealed taxonomic shifts including an increase in Akkermansia and a decrease in Proteobacteria. These changes were independent of age, weight, fat % as well as energy and fiber intake. Training slightly increased Jaccard distance of genus level β-diversity. Training did not alter the enriched metagenomic pathways, which, according to Bray Curtis dissimilarity analysis, may have been due to that only half of the subjects' microbiomes responded considerably to exercise. Nevertheless, tranining decreased the abundance of several genes including those related to fructose and amino acid metabolism. These metagenomic changes, however, were not translated into major systemic metabolic changes as only two metabolites, phospholipids and cholesterol in large VLDL particles, decreased after exercise. Training also decreased the amine oxidase activity of pro-inflammatory VAP-1, whereas no changes in CRP were detected. All clinical blood variables were within normal range, yet exercise slightly increased glucose and decreased LDL and HDL. In conclusion, exercise training modified the gut microbiome without greatly affecting systemic metabolites or body composition. Based on our data and existing literature, we propose that especially Akkermansia and Proteobacteria are exercise-responsive taxa. Our results warrant the need for further studies in larger cohorts to determine whether exercise types other than endurance exercise also modify the gut metagenome.
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spelling pubmed-61789022018-10-18 Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women Munukka, Eveliina Ahtiainen, Juha P. Puigbó, Pere Jalkanen, Sirpa Pahkala, Katja Keskitalo, Anniina Kujala, Urho M. Pietilä, Sami Hollmén, Maija Elo, Laura Huovinen, Pentti D'Auria, Giuseppe Pekkala, Satu Front Microbiol Microbiology Recent studies suggest that exercise alters the gut microbiome. We determined whether six-weeks endurance exercise, without changing diet, affected the gut metagenome and systemic metabolites of overweight women. Previously sedentary overweight women (n = 19) underwent a six-weeks endurance exercise intervention, but two were excluded due to antibiotic therapy. The gut microbiota composition and functions were analyzed by 16S rRNA gene amplicon sequencing and metagenomics. Body composition was analyzed with DXA X-ray densitometer and serum metabolomics with NMR metabolomics. Total energy and energy-yielding nutrient intakes were analyzed from food records using Micro-Nutrica software. Serum clinical variables were determined with KONELAB instrument. Soluble Vascular Adhesion Protein 1 (VAP-1) was measured with ELISA and its' enzymatic activity as produced hydrogen peroxide. The exercise intervention was effective, as maximal power and maximum rate of oxygen consumption increased while android fat mass decreased. No changes in diet were observed. Metagenomic analysis revealed taxonomic shifts including an increase in Akkermansia and a decrease in Proteobacteria. These changes were independent of age, weight, fat % as well as energy and fiber intake. Training slightly increased Jaccard distance of genus level β-diversity. Training did not alter the enriched metagenomic pathways, which, according to Bray Curtis dissimilarity analysis, may have been due to that only half of the subjects' microbiomes responded considerably to exercise. Nevertheless, tranining decreased the abundance of several genes including those related to fructose and amino acid metabolism. These metagenomic changes, however, were not translated into major systemic metabolic changes as only two metabolites, phospholipids and cholesterol in large VLDL particles, decreased after exercise. Training also decreased the amine oxidase activity of pro-inflammatory VAP-1, whereas no changes in CRP were detected. All clinical blood variables were within normal range, yet exercise slightly increased glucose and decreased LDL and HDL. In conclusion, exercise training modified the gut microbiome without greatly affecting systemic metabolites or body composition. Based on our data and existing literature, we propose that especially Akkermansia and Proteobacteria are exercise-responsive taxa. Our results warrant the need for further studies in larger cohorts to determine whether exercise types other than endurance exercise also modify the gut metagenome. Frontiers Media S.A. 2018-10-03 /pmc/articles/PMC6178902/ /pubmed/30337914 http://dx.doi.org/10.3389/fmicb.2018.02323 Text en Copyright © 2018 Munukka, Ahtiainen, Puigbó, Jalkanen, Pahkala, Keskitalo, Kujala, Pietilä, Hollmén, Elo, Huovinen, D'Auria and Pekkala. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Munukka, Eveliina
Ahtiainen, Juha P.
Puigbó, Pere
Jalkanen, Sirpa
Pahkala, Katja
Keskitalo, Anniina
Kujala, Urho M.
Pietilä, Sami
Hollmén, Maija
Elo, Laura
Huovinen, Pentti
D'Auria, Giuseppe
Pekkala, Satu
Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women
title Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women
title_full Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women
title_fullStr Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women
title_full_unstemmed Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women
title_short Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women
title_sort six-week endurance exercise alters gut metagenome that is not reflected in systemic metabolism in over-weight women
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6178902/
https://www.ncbi.nlm.nih.gov/pubmed/30337914
http://dx.doi.org/10.3389/fmicb.2018.02323
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