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Prolonged restraint stressor exposure in outbred CD-1 mice impacts microbiota, colonic inflammation, and short chain fatty acids

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Maltz, Ross M., Keirsey, Jeremy, Kim, Sandra C., Mackos, Amy R., Gharaibeh, Raad Z., Moore, Cathy C., Xu, Jinyu, Bakthavatchalu, Vasudevan +2 more·2018·PLOS ONE
DOI 10.1371/journal.pone.0196961PMC PMC5942810
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Abstract

Stressor-exposure has been shown to exacerbate inflammation and change the composition of the gastrointestinal microbiota; however stressor-induced effects on microbiota-derived metabolites and their receptors are unknown. Thus, bacterial-produced short chain fatty acids (SCFAs), as well as microbial community composition, were assessed in the colons of mice exposed to stress during infection with Citrobacter rodentium. Mice were exposed to overnight restraint on 7 consecutive nights, or left undisturbed as a control. After the first exposure of restraint, mice were orally challenged with C. rodentium or with vehicle. Microbial community composition was assessed using 16S rRNA gene sequencing and SCFA levels measured using gas chromatography-mass spectrometry (GC-MS). Pathogen levels and colonic inflammation were also assessed 6 days post-infection. Results demonstrated that the microbial community structure and SCFA production were significantly affected by both stressor exposure and C. rodentium-infection. Exposure to prolonged restraint in the absence of infection significantly reduced SCFAs (acetic acid, butyric acid, and propionic acid). Multiple bacterial taxa were affected by stressor exposure, with the relative abundance of Lactobacillus being significantly reduced and directly correlated with propionic acid. Lactobacillus abundances were inversely correlated with colonic inflammation, supporting the contention that Lactobacillus helps to regulate mucosal inflammatory responses. Our data indicates that restraint stressor can have significant effects on pathogen-induced colonic inflammation and suggest that stressor-induced changes in the microbiota, microbial-produced SCFAs and their receptors may be involved.

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  • In some studies, decreased gastrointestinal SCFA levels have been associated with chronic stress.

    “and in some studies chronic stress, including (Maltz et al., 2018).”

    From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Maltz et al., 2018

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Authors
Maltz, R. M., Keirsey, J., Kim, S. C., Mackos, A. R., Gharaibeh, R. Z., Moore, C. C., Xu, J., Bakthavatchalu, V., Somogyi, A., & Bailey, M. T.
Affiliations
  • Nationwide Children's Hospital (US)
  • The Ohio State University (US)
  • University of North Carolina at Charlotte (US)
  • Massachusetts Institute of Technology (US)
Corresponding author
Maltz, Ross M.
ORCID
Venue
PLOS ONE
Publisher
Public Library of Science (PLoS)
Published
2018-05-09
Volume
13
Issue
5
Pages
e0196961
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0196961
PMC
PMC5942810
OpenAlex
W2800822268
Cited by
51
References
6
Citations by year
2026: 1 · 2025: 6 · 2024: 4 · 2023: 5 · 2022: 12 · 2021: 11 · 2020: 3 · 2019: 7 · 2018: 2
FWCI
2.05
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Center for Complementary and Integrative Health (R01AT006552)
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
restraint stress, psychological stress, gut microbiota, short-chain fatty acids, colonic inflammation, Citrobacter rodentium infection, Lactobacillus, propionic acid, butyrate, acetic acid, microbial metabolites, mucosal inflammation, ICR mice
MeSH terms
Gastrointestinal Microbiome, Animals, Colon, Enterobacteriaceae Infections, Fatty Acids, Volatile, Inflammation, Intestinal Mucosa, Lactobacillus, Restraint, Physical, RNA, Ribosomal, 16S, Citrobacter rodentium, Mice, Microbiota

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