The DOI matches its Crossref record; 53 of the 53 references it cites were found in a registry or an index.
Stressor Exposure Disrupts Commensal Microbial Populations in the Intestines and Leads to Increased Colonization by Citrobacter rodentium
Open accessAbstract
The gastrointestinal tract is colonized by an enormous array of microbes that are known to have many beneficial effects on the host. Previous studies have indicated that stressor exposure can disrupt the stability of the intestinal microbiota, but the extent of these changes, as well as the effects on enteric infection, has not been well characterized. In order to examine the ability of stressors to induce changes in the gut microbiota, we exposed mice to a prolonged restraint stressor and then characterized microbial populations in the intestines using both traditional culture techniques and bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). Exposure to the stressor led to an overgrowth of facultatively anaerobic microbiota while at the same time significantly reducing microbial richness and diversity in the ceca of stressed mice. Some of these effects could be explained by a stressor-induced reduction in the relative abundance of bacteria in the family Porphyromonadaceae . To determine whether these alterations would lead to increased pathogen colonization, stressed mice, as well as nonstressed controls, were challenged orally with the enteric murine pathogen Citrobacter rodentium . Exposure to the restraint stressor led to a significant increase in C. rodentium colonization over that in nonstressed control mice. The increased colonization was associated with increased tumor necrosis factor alpha (TNF-α) gene expression in colonic tissue. Together, these data demonstrate that a prolonged stressor can significantly change the composition of the intestinal microbiota and suggest that this disruption of the microbiota increases susceptibility to an enteric pathogen.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Similarly, psychosocial stressors can change the composition of the intestinal microbiota and affect the brain-gut axis function (6, 7, 119).”
From Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome (2013) · cites this paper as [7]
In the citing paper
“In both a human-associated microbiota43-45 and macroecological46,47 context, higher phylogenetic diversity is associated with greater ecosystem resilience and productivity.”
From Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions (2013) · cites this paper as [43]
In the citing paper
“When challenged orally with the enteric murine pathogen C. rodentium, chronically stressed mice had an increased pathogen load and increased colonic TNF-α expression.”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [359]
In the citing paper
“Mice exposed to prolonged restraint stress demonstrated changes in GM composition, such as bacterial overgrowth and reductions in diversity and richness (359).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [359]
In the citing paper
“Probiotics rescued these changes in the GM and the associated host-microbe interactions.”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [359]
Citations
Cites
A core gut microbiome in obese and lean twins
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009) · Nature · doi:10.1038/nature07540 · Cited by 7,823
The Ribosomal Database Project: improved alignments and new tools for rRNA analysis
Cole, J. R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R. J., Kulam-Syed-Mohideen, A. S., McGarrell, D. M., Marsh, T. L., Garrity, G. M., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn879 · Cited by 4,873
Metagenomic Analysis of the Human Distal Gut Microbiome
Gill, S. R., Pop, M., DeBoy, R. T., Eckburg, P. B., Turnbaugh, P. J., Samuel, B. S., Gordon, J. I., Relman, D. A., Fraser-Liggett, C. M., & Nelson, K. E. (2006) · Science · doi:10.1126/science.1124234 · Cited by 4,699
The gut flora as a forgotten organ
O'Hara, A. M., & Shanahan, F. (2006) · The EMBO Reports · doi:10.1038/sj.embor.7400731 · Cited by 2,791
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638 · cited 1×
“hypothalamic-pituitary-adrenal axis (35, 45).”
Lupp, C., Robertson, M. L., Wickham, M. E., Sekirov, I., Champion, O. L., Gaynor, E. C., & Finlay, B. B. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.06.010 · Cited by 1,310
Dowd, S. E., Callaway, T. R., Wolcott, R. D., Sun, Y., McKeehan, T., Hagevoort, R. G., & Edrington, T. S. (2008) · BMC Microbiology · doi:10.1186/1471-2180-8-125 · Cited by 1,121 · cited 1×
“software (16) and the Black Box Chimera Check software B2C2 (described and”
MethodSelf-citationKassinen, A., Krogius-Kurikka, L., Mäkivuokko, H., Rinttilä, T., Paulin, L., Corander, J., Malinen, E., Apajalahti, J., & Palva, A. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.04.005 · Cited by 1,002
Colonization resistance of the digestive tract in conventional and antibiotic-treated mice
van der Waaij, D., Vries, J. M. B.-D., & der Wees, J. E. C. L.-V. (1971) · Journal of Hygiene · doi:10.1017/s0022172400021653 · Cited by 907
Reproducible Community Dynamics of the Gastrointestinal Microbiota following Antibiotic Perturbation
Antonopoulos, D. A., Huse, S. M., Morrison, H. G., Schmidt, T. M., Sogin, M. L., & Young, V. B. (2009) · Infection and Immunity · doi:10.1128/iai.01520-08 · Cited by 564
Cited by
Sorted by citations
Items 301–335 of 335
Mercer, E. M., Piché‐Choquette, S., Gorospe, J., Rangipour, Z., Asbury, M. R., Alshaikh, B. N., Sycuro, L. K., Kembel, S. W., Giesbrecht, G. F., & Arrieta, M. (2025) · Gut Microbiology · doi:10.1016/j.gutmic.2025.100004 · Cited by 1
Intestinal microbiota and stress: how much do we know so far
Hyder, N., & Raza, M. L. (2026) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2026.2706149 · Cited by 1
Intersections Between Neuroimmune and Microbiota
Ndjom, C. G. N., Gonzalez, X. F., & Jones, H. P. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7828-1_2 · Cited by 1
Spinal cord injury and the gut microbiota
Kigerl, K. A., & Popovich, P. G. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-822427-4.00036-8 · Cited by 1
Su, R., & Yang, Y. (2023) · Parasitology Research · doi:10.1007/s00436-023-07962-9 · Cited by 1
Commensal Gastrointestinal Microbiota as a Complex Interactive Consortia
Patterson, J. A., Callaway, T. R., & Ricke, S. C. (2023) · Springer eBooks · doi:10.1007/978-3-031-40512-9_1 · Cited by 1
Foster, J. A., & Clarke, G. A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-814800-6.00008-x · Cited by 1
The microbiome and host behaviour
Lizé, A., & Lewis, Z. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108654418.006 · Cited by 1
Wang, Y., Yu, L., Li, X., Chen, H., Ren, P., Li, N., & Jiang, L. (2023) · Research Square · doi:10.21203/rs.3.rs-3081793/v1 · Cited by 1
Chen, L. (2012) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Exploring the breadth and depth of diversity within the canine gut microbiome
Hand, D. (2011) · University of Birmingham Institutional Research Archive (University of Birmingham)
Neuroendocrine-Immune Interactions in Neurotropic Viral Infections
Welsh, C. J., Steelman, A. J., Young, C. R., Linsenbardt, H. R., & Meagher, M. W. (2016) · Springer eBooks · doi:10.1007/978-3-319-33189-8_9
Impact of antibiotic use, alternative therapies and inflammation on the intestinal microbiota
Overstreet, A.-M. C. (2012) · Iowa State University Digital Repository (Iowa State University) · doi:10.31274/etd-180810-1992
Defining stress-induced systemic sterile inflammatory responses: Network, signals, and pathways
Maslanik, T. (2012) · CU Scholar (University of Colorado Boulder)
Future Development of Infectious Microecology
Li, L., & Chen, Y. (2014) · Advanced topics in science and technology in China · doi:10.1007/978-3-662-43883-1_23
Parental and Early Developmental Stress Impact on Neurodevelopmental and Neuropsychiatric Disorders
Nugent, B. M., Chan, J. C., Jašarević, E., & Bale, T. L. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00097-3
Cook, M. D. (2013) · Illinois Digital Environment for Access to Learning and Scholarship (University of Illinois at Urbana-Champaign)
Medication management in pediatric chronic illness: Should patient anxiety be considered?
Hoogendoorn, C. J. (2016) · CUNY Academic Works (City University of New York)
microbial community in a high Arctic hypersaline subzero spring 2
Lay, C.-Y., Mykytczuk, N., Yergeau, É., Guillaume, Greer, C. W., & Whyte, L. G. (2013)
[Progresses on the effects and mechanisms of stress on gut microbiota].
Song, L., Zhang, J., & Duan, L.-P. (2020) · PubMed
Underlying mechanisms for intestinal diseases arising from stress
Li, J., Ren, W., Yin, H., Zhao, Y.-F., & Tang, Y. (2020) · World Chinese Journal of Digestology · doi:10.11569/wcjd.v28.i14.617
Molecular mechanisms of neurodegeneration in neurotraumatic diseases
Farooqui, A. A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-821711-5.00003-6
Social relationships: key to gut microbiome composition in wild redfronted lemurs?
Corrales, S. T. M. (2022) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7766
Soil intake modifies the gut microbiota and alleviates ovalbumin-induced mice asthma inflammationPreprint
Li, M., Li, N., Dong, Y., Zhang, H., Bai, Z., Zhang, R., Fei, Z., Zhu, W., Xiao, P., Sun, X. S., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.31.543010
Lourenco, J. M., & Callaway, T. R. (2024) · Microorganisms · doi:10.3390/microorganisms12050859
FW, F. N. F. L. N. F. L. N. F. L. N. F. L. N., & 11, C. N. F. (2019) · doi:10.1472/noissn1472_monp_testmedra_cit_ref
Fenn, J., Taylor, C. H., Goertz, S., Wanelik, K. M., Paterson, S., Begon, M., Jackson, J., & Bradley, J. (2024) · Figshare · doi:10.6084/m9.figshare.26579084
Liu, M., Gao, C., Cao, Y., Sun, J., & Zhang, Z. (2026) · Genes & Diseases · doi:10.1016/j.gendis.2026.102106
Challenges associate with microbiome diversity, glucocorticoids, and condition in a wild songbird
Slevin, M. C., Houtz, J. L., Vitousek, M. N., & Anderson, R. C. (2026) · Scientific Reports · doi:10.1038/s41598-026-42507-x
Iachizzi, M., Zajac, N., Ruiz, J. L., Güller, T., RABIN, R., Schalbetter, S. M., Cillis, F. D., Moccia, M., Cattaneo, A., Cryan, J. F., et al. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106571
Schiele, J., Tsai, P.-L., Schimmele, T., Beck, S., Meyer, M., Mannes, M., Desmond, L. W., Noschka, R., Huber-Lang, M. S., Haffner‐Luntzer, M., et al. (2026) · Molecular Psychiatry · doi:10.1038/s41380-026-03638-9
Zhang, L., Ni, L., Pan, L., Cao, R., Han, L., & Long, L. (2026) · Frontiers in Microbiology · doi:10.3389/fmicb.2026.1851267
Liu, A., Ai, Y., Yang, P.-C., Zhang, L., Hong, G., Schnabl, B., Xu, K.-S., Cai, K.-L., Hou, X., & Chu, H.-K. (2026) · Journal of Advanced Research · doi:10.1016/j.jare.2026.08.010
Metadata
- Authors
- Bailey, M. T., Dowd, S. E., Parry, N. M. A., Galley, J. D., Schauer, D. B., & Lyte, M.
- Affiliations
- The Ohio State University (US)
- Research and Testing Laboratory and Medical Biofilm Research Institute, Lubbock, Texas 79407
- Massachusetts Institute of Technology (US)
- Texas Tech University (US)
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 2010-04
- Volume
- 78
- Issue
- 4
- Pages
- 1509-1519
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- PMC
- PMC2849416
- OpenAlex
- W2143862999
- Cited by
- 335
- References
- 53
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 18 · 2023: 17 · 2022: 26 · 2021: 21 · 2020: 15 · 2019: 19 · 2018: 22 · 2017: 22 · 2016: 26 · 2015: 17 · 2014: 29 · 2013: 27 · 2012: 26
- FWCI
- 10.94
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Infection and Immunity (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Texas Tech University
- National Institute of Allergy and Infectious Diseases (R03AI069097)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Keywords
- restraint stress, gut microbiota, gut dysbiosis, Citrobacter rodentium, gastrointestinal infections, Porphyromonadaceae, microbial diversity, TNF-alpha gene expression, commensal bacteria, host susceptibility to infection, cecal microbiota
- MeSH terms
- Animals, Bacteria, Enterobacteriaceae Infections, Male, Stress, Physiological, Colony Count, Microbial, Gastrointestinal Tract, Citrobacter rodentium, Biodiversity, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review