Cited by 373Gut microbiota and healthGastrointestinal motility and disordersProbiotics and Fermented Foods

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Changes in intestinal microbiota composition and metabolism coincide with increased intestinal permeability in young adults under prolonged physiological stress

Karl, J. Philip, Margolis, Lee M., Madslien, Elisabeth H., Murphy, Nancy E., Castellani, John W., Gundersen, Yngvar, Hoke, Allison V., Levangie, Michael W., Kumar, Raina, Chakraborty, Nabarun, Gautam, Aarti, Hammamieh, Rasha, Martini, Svein, Montain, Scott J., Pasiakos, Stefan M.·2017·American Journal of Physiology-Gastrointestinal and Liver Physiology

DOI 10.1152/ajpgi.00066.2017

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Abstract

The magnitude, temporal dynamics, and physiological effects of intestinal microbiome responses to physiological stress are poorly characterized. This study used a systems biology approach and a multiple-stressor military training environment to determine the effects of physiological stress on intestinal microbiota composition and metabolic activity, as well as intestinal permeability (IP). Soldiers ( n = 73) were provided three rations per day with or without protein- or carbohydrate-based supplements during a 4-day cross-country ski-march (STRESS). IP was measured before and during STRESS. Blood and stool samples were collected before and after STRESS to measure inflammation, stool microbiota, and stool and plasma global metabolite profiles. IP increased 62 ± 57% (mean ± SD, P < 0.001) during STRESS independent of diet group and was associated with increased inflammation. Intestinal microbiota responses were characterized by increased α-diversity and changes in the relative abundance of >50% of identified genera, including increased abundance of less dominant taxa at the expense of more dominant taxa such as Bacteroides. Changes in intestinal microbiota composition were linked to 23% of metabolites that were significantly altered in stool after STRESS. Together, pre-STRESS Actinobacteria relative abundance and changes in serum IL-6 and stool cysteine concentrations accounted for 84% of the variability in the change in IP. Findings demonstrate that a multiple-stressor military training environment induced increases in IP that were associated with alterations in markers of inflammation and with intestinal microbiota composition and metabolism. Associations between IP, the pre-STRESS microbiota, and microbiota metabolites suggest that targeting the intestinal microbiota could provide novel strategies for preserving IP during physiological stress. NEW & NOTEWORTHY Military training, a unique model for studying temporal dynamics of intestinal barrier and intestinal microbiota responses to stress, resulted in increased intestinal permeability concomitant with changes in intestinal microbiota composition and metabolism. Prestress intestinal microbiota composition and changes in fecal concentrations of metabolites linked to the microbiota were associated with increased intestinal permeability. Findings suggest that targeting the intestinal microbiota could provide novel strategies for mitigating increases in intestinal permeability during stress.

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Authors: Karl, J. P., Margolis, L. M., Madslien, E. H., Murphy, N. E., Castellani, J. W., Gundersen, Y., Hoke, A. V., Levangie, M. W., Kumar, R., Chakraborty, N., Gautam, A., Hammamieh, R., Martini, S., Montain, S. J., & Pasiakos, S. M.
Affiliations: U.S. Army Research Institute of Environmental Medicine (US)
Norwegian Defence Research Establishment (NO)
United States Army (US)
Frederick National Laboratory for Cancer Research (US)
Corresponding author: Karl, J. Philip
ORCID: Karl, J. Philip
Margolis, Lee M.
Madslien, Elisabeth H.
Murphy, Nancy E.
Castellani, John W.
Hoke, Allison V.
Kumar, Raina
Chakraborty, Nabarun
Gautam, Aarti
Hammamieh, Rasha
Martini, Svein
Pasiakos, Stefan M.
Venue: American Journal of Physiology-Gastrointestinal and Liver Physiology
Publisher: American Physiological Society
Published: 2017-06-01
Volume: 312
Issue: 6
Pages: G559-G571
ISSN: 0193-1857 (ISSN-L)
1522-1547
DOI: 10.1152/ajpgi.00066.2017
OpenAlex: W2600336120
Cited by: 373
References: 57
Citations by year: 2026: 27 · 2025: 41 · 2024: 46 · 2023: 55 · 2022: 47 · 2021: 49 · 2020: 42 · 2019: 28 · 2018: 27 · 2017: 10
FWCI: 11.95
Type: journal article
Language: en
Open access: closed
Locations: American Journal of Physiology-Gastrointestinal and Liver Physiology (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. Army Medical Research and Materiel Command
Defense Health Agency
Norwegian Defense Research Establishment
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Keywords: gut microbiota, intestinal permeability, physiological stress, military education, intestinal barrier, inflammation, microbiota metabolites, actinobacteria, Bacteroides, cysteine, interleukin-6, young adults
MeSH terms: Gastrointestinal Microbiome, Adolescent, Age Factors, Bacteria, Dietary Carbohydrates, Dietary Proteins, Energy Metabolism, Feces, Female, Humans, Intestinal Absorption, Intestinal Mucosa, Intestines, Male, Military Medicine, Norway, Nutritional Status, Permeability, Physical Endurance, Stress, Physiological, Time Factors, Inflammation Mediators, Systems Biology, Host-Pathogen Interactions, Metabolomics, Young Adult

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Changes in intestinal microbiota composition and metabolism coincide with increased intestinal permeability in young adults under prolonged physiological stress

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