Changes in intestinal microbiota composition and metabolism coincide with increased intestinal permeability in young adults under prolonged physiological stress
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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Individuals who performed a 4-day cross-country ski-march in Arctic conditions had increased microbial diversity compared to controls.
“An increase of microbial diversity was once again reported in individuals who performed a 4-day cross-country ski-march in Arctic conditions compared to controls, by (Karl et al., 2017), amongst other changes.”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Karl et al., 2017
Psychological stress, physical activity, tobacco use, alcohol consumption, and antibiotic exposure are modifying factors for the gut microbiome.
“Other modifying factors (Figure 1) include psychological stress33,34, physical activity35, tobacco use36, alcohol consumption37, and antibiotic exposure38, 39,40.”
From The gut Microbiome in adult and pediatric functional gastrointestinal disorders (2019) · cites this paper as [34]
A 4-day cross-country, military ski-march increased Verrucomicrobia abundance.
“Second, a 4-days cross-country, military ski-march increased Verrucomicrobia abundance (Karl et al., 2017)”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Karl et al., 2017
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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
- 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
- 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 · 2016: 1
- 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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