The enteric nervous system promotes intestinal health by constraining microbiota composition
Open accessAbstract
Sustaining a balanced intestinal microbial community is critical for maintaining intestinal health and preventing chronic inflammation. The gut is a highly dynamic environment, subject to periodic waves of peristaltic activity. We hypothesized that this dynamic environment is a prerequisite for a balanced microbial community and that the enteric nervous system (ENS), a chief regulator of physiological processes within the gut, profoundly influences gut microbiota composition. We found that zebrafish lacking an ENS due to a mutation in the Hirschsprung disease gene, sox10, develop microbiota-dependent inflammation that is transmissible between hosts. Profiling microbial communities across a spectrum of inflammatory phenotypes revealed that increased levels of inflammation were linked to an overabundance of pro-inflammatory bacterial lineages and a lack of anti-inflammatory bacterial lineages. Moreover, either administering a representative anti-inflammatory strain or restoring ENS function corrected the pathology. Thus, we demonstrate that the ENS modulates gut microbiota community membership to maintain intestinal health.
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In zebrafish lacking an ENS due to a sox10 mutation, a pro-inflammatory microbiota profile developed, and its effects could be ameliorated by transplantation of wild-type ENS precursors or by introduction of anti-inflammatory microbes.
“In zebrafish lacking an ENS as a consequence of a mutation in an SRY-related HMG-box (sox10 transcription factor gene), a 'pro-inflammatory' microbiota profile developed, the effects of which could be ameliorated by transplantation of wild-type ENS precursors into sox10 mutants or by the introduction of 'anti-inflammatory' microbes (Rolig et al., 2017).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Rolig et al., 2017
The ENS appears to be able to exert control over the gut microbiota.
“the ENS appears to be able to exert control of the microbiota (Rolig et al., 2017).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Rolig et al., 2017
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- Authors
- Rolig, A. S., Mittge, E. K., Ganz, J., Troll, J. V., Melancon, E., Wiles, T. J., Alligood, K., Stephens, W. Z., Eisen, J. S., & Guillemin, K.
- Affiliations
- University of Oregon (US)
- Canadian Institute for Advanced Research (CA)
- Corresponding author
- Eisen, Judith S.
- Guillemin, Karen
- Venue
- PLOS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2017-02-16
- Volume
- 15
- Issue
- 2
- Pages
- e2000689
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC5331947
- OpenAlex
- W2588467249
- Cited by
- 152
- References
- 69
- Citations by year
- 2026: 14 · 2025: 5 · 2024: 15 · 2023: 18 · 2022: 13 · 2021: 18 · 2020: 20 · 2019: 21 · 2018: 19 · 2017: 9
- FWCI
- 7.71
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- John Simon Guggenheim Memorial Foundation
- University of Oregon (P01HD22486, P50GM098911)
- National Institute of General Medical Sciences (T32GM007413, P50GM098911, P01HD22486)
- National Institute of Diabetes and Digestive and Kidney Diseases (F32DK098884)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01HD022486)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Health Sciences › Medicine › Surgery › Congenital gastrointestinal and neural anomalies
- Keywords
- enteric nervous system, gut microbiota, gut health, Hirschsprung disease, SOX10, intestinal inflammation, peristalsis, zebrafish, anti-inflammatory bacteria, pro-inflammatory bacteria, host-to-host transmission, intestinal motility
- MeSH terms
- Gastrointestinal Microbiome, Animals, Bacteria, Cell Count, Gene Expression Regulation, Inflammation, Intestines, Leukocyte Count, Models, Biological, Mutation, Neutrophils, Phylogeny, Zebrafish, Colony Count, Microbial, Enteric Nervous System, Zebrafish Proteins, Stem Cell Transplantation, SOXE Transcription Factors, Dysbiosis
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