Healthy hosts rule within: ecological forces shaping the gut microbiota

Byndloss, Mariana X.; Pernitzsch, Sandy R.; Bäumler, Andreas J.

doi:10.1038/s41385-018-0010-y

Cited by 110Gut microbiota and healthGastrointestinal motility and disordersAnimal Nutrition and Physiology

Healthy hosts rule within: ecological forces shaping the gut microbiota

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Byndloss, Mariana X., Pernitzsch, Sandy R., Bäumler, Andreas J.·2018·Mucosal Immunology

DOI 10.1038/s41385-018-0010-y

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Abstract

A balanced gut microbiota is important for human health, but the mechanisms that maintain homeostasis are incompletely understood. Recent insights suggest the host plays a key role in shaping its gut microbiota to be beneficial. While host control in the small intestine curbs bacterial numbers to avoid competition for simple sugars and amino acids, the host limits oxygen availability in the large intestine to obtain microbial fermentation products from fiber. Epithelial cells are major players in imposing ecological control mechanisms, which involves the release of antimicrobial peptides by small-intestinal Paneth cells and maintenance of luminal anaerobiosis by epithelial hypoxia in the colon. Harnessing these epithelial control mechanisms for therapeutic means could provide a novel lynchpin for strategies to remediate dysbiosis.

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Oxygen availability during inflammation drives dysbiosis by favoring Enterobacteriaceae expansion through respiration.
“For example, the availability of oxygen during inflammation drives a disruption, or dysbiosis, of the microbiota by favoring Enterobacteriaceae expansion through respiration (Byndloss et al., 2018).”
From The Impact of Dietary Transition Metals on Host-Bacterial Interactions (2018) · cites this paper as Byndloss et al., 2018

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Consensus report: faecal microbiota transfer – clinical applications and procedures
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Commensal Koch's postulates: establishing causation in human microbiota research
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Intestinal Metabolism and Transport of 5-Aminosalicylate
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Mesalazine A Review of its Pharmacodynamic and Pharmacokinetic Properties, and Therapeutic Potential in Chronic Inflammatory Bowel Disease
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Faecal microbiota transplantation: applications and limitations in treating gastrointestinal disorders
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Decreased Paneth cell defensin expression in ileal Crohn's disease is independent of inflammation, but linked to the NOD2 1007fs genotype.
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Die Aetiologie der Tuberkulose
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Management of acute severe ulcerative colitis
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Can fecal microbiota transplantation cure irritable bowel syndrome?
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Gastric intrinsic factor: The gastric and small intestinal stages of cobalamin absorption. A personal journey
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Mesalazine for the treatment of inflammatory bowel disease
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The dual nature of haemocyanin in the establishment and persistence of the squid–vibrio symbiosis
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Bactericidal Permeability-Increasing Proteins Shape Host-Microbe Interactions
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Microbial Therapeutics Designed for Infant Health
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ATG16L1 Crohn's disease risk stresses the endoplasmic reticulum of Paneth cells
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Non‐native acylated homoserine lactones reveal that LuxIR quorum sensing promotes symbiont stability
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2 of the 106 references couldn’t be matched to a known paper.

Sorted by citations

Gut microbiome stability and resilience: elucidating the response to perturbations in order to modulate gut health
Fassarella, M., Blaak, E. E., Penders, J., Nauta, A., Smidt, H., & Zoetendal, E. G. (2020) · Gut · doi:10.1136/gutjnl-2020-321747 · Cited by 781 · see citing works
“54 Additionally, the acidic pH found in the stomach is considered a first line of protection against foreign microbes, 55 and the bile acids, secreted at the proximal end of the small intestine, are bactericidal to certain species and known to broadly shape the composition of the microbiota.”
Background
The microbiome and gut homeostasis
Lee, J., Tsolis, R. M., & Bäumler, A. J. (2022) · Science · doi:10.1126/science.abp9960 · Cited by 430 · see citing works
Bile acids as modulators of gut microbiota composition and function
Larabi, A. B., Masson, H. L. P., & Bäumler, A. J. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2172671 · Cited by 412 · see citing works
The microbiome-shaping roles of bacteriocins
Heilbronner, S., Krismer, B., Brötz‐Oesterhelt, H., & Peschel, A. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-021-00569-w · Cited by 398 · see citing works
The Healthy Microbiome—What Is the Definition of a Healthy Gut Microbiome?
Shanahan, F., Ghosh, T. S., & O’Toole, P. W. (2021) · Gastroenterology · doi:10.1053/j.gastro.2020.09.057 · Cited by 383 · see citing works
The Association between Early-Life Gut Microbiota and Long-Term Health and Diseases
Sarkar, A., Yoo, J. Y., Dutra, S. V. O., Morgan, K. H., & Groer, M. E. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10030459 · Cited by 346 · see citing works
“Changes in bacteria composition and diversity can lead to disruption in the epithelial barrier and increase susceptibility to infections and immune disorders [94-96].”
Background
Mining the microbiota for microbial and metabolite-based immunotherapies
Skelly, A. N., Sato, Y., Kearney, S., & Honda, K. (2019) · Nature Reviews Immunology · doi:10.1038/s41577-019-0144-5 · Cited by 306 · see citing works
Advancing human gut microbiota research by considering gut transit time
Procházková, N., Falony, G., Dragsted, L. O., Licht, T. R., Raes, J., & Roager, H. M. (2022) · Gut · doi:10.1136/gutjnl-2022-328166 · Cited by 322 · see citing works
RETRACTED: Effects of berberine and metformin on intestinal inflammation and gut microbiome composition in db/db mice
Zhang, W., Xu, J., Yu, T., & Chen, Q. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2019.109131 · Cited by 242 · see citing works
Retracted
The Impact of Dietary Transition Metals on Host-Bacterial Interactions
Lopez, C. A., & Skaar, E. P. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.05.008 · Cited by 190 · see citing works
“, 2002; Janakiraman and Slauch, 2000), in part by providing iron to iron-sulfur (FeS) clusters necessary for respiration (Byndloss et al., 2018).”
Background
Synthetic ecology of the human gut microbiota
Vrancken, G., Gregory, A., Huys, G. R. B., Faust, K., & Raes, J. (2019) · Nature Reviews Microbiology · doi:10.1038/s41579-019-0264-8 · Cited by 192 · see citing works
Gut dysbiosis: Ecological causes and causative effects on human disease
Winter, S., & Bäumler, A. J. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2316579120 · Cited by 150 · see citing works
“This paradigm shift suggests that dysbiosis represents a state of weakened host control over the microbial environment, whereas gut homeostasis defines a state where these host functions operate normally (24, 63, 65, 68).”
Background
Prenatal and postnatal contributions of the maternal microbiome on offspring programming
Jašarević, E., & Bale, T. L. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100797 · Cited by 127 · see citing works
Editing of the gut microbiota reduces carcinogenesis in mouse models of colitis-associated colorectal cancer
Zhu, W., Miyata, N., Winter, M. G., Arenales, A., Hughes, E. R., Spiga, L., Kim, J., Sifuentes-Dominguez, L., Starokadomskyy, P., Gopal, P., et al. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20181939 · Cited by 124 · see citing works
Dysbiosis: from fiction to function
Tiffany, C. R., & Bäumler, A. J. (2019) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00230.2019 · Cited by 122 · see citing works
“ota, which is shaped by the human host (10, 17).”
Background
Swimming Motility and Chemotaxis Control the Spatial Organization, Persistence, and Inflammatory Activity of a Model Intestinal Pathobiont
Wiles, T. J., Schlomann, B. H., Wall, E. S., Betancourt, R., Parthasarathy, R., & Guillemin, K. J. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000661 · Cited by 95 · see citing works
The composition of human vaginal microbiota transferred at birth affects offspring health in a mouse model
Jašarević, E., Hill, E. M., Kane, P. J., Rutt, L., Gyles, T. M., Folts, L. M., Rock, K. D., Howard, C. D., Morrison, K. E., Ravel, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26634-9 · Cited by 85 · see citing works
Modulation of microbially derived short-chain fatty acids on intestinal homeostasis, metabolism, and neuropsychiatric disorder
Xiao, S., Jiang, S., Qian, D., & Duan, J. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-10312-4 · Cited by 84 · see citing works
Diet-Microbe-Host Interactions That Affect Gut Mucosal Integrity and Infection Resistance
Forgie, A. J., Fouhse, J. M., & Willing, B. P. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01802 · Cited by 85 · see citing works
Neonatal Vitamin A Supplementation and Vitamin A Status Are Associated with Gut Microbiome Composition in Bangladeshi Infants in Early Infancy and at 2 Years of Age.
Huda, M., Ahmad, S. M., Kalanetra, K., Taft, D. H., Alam, M. J., Khanam, A., Raqib, R., Underwood, M. A., Mills, D., & Stephensen, C. B. (2019) · Journal of NutriLife · doi:10.1093/jn/nxz034 · Cited by 58 · see citing works
“It is also possible that VAS could promote normal development of the colonic epithelial barrier (9–12), or enhance its repair after damage (14–16), to maintain an appropriate, low oxygen tension in the colonic lumen (59).”
Background
Deciphering the gut microbiome of grass carp through multi-omics approach
Li, M., Liang, H., Yang, H., Ding, Q., Xia, R., Chen, J., Zhou, W., Yang, Y., Zhang, Z., Yao, Y., et al. (2024) · Microbiome · doi:10.1186/s40168-023-01715-7 · Cited by 77 · see citing works
“The important role of the commensal microbiota in immune homeostasis, disease and 42 health has been demonstrated in humans [7-9], and a comprehensive gut microbiome gene 43”
Background
Anaerobic Respiration of NOX1-Derived Hydrogen Peroxide Licenses Bacterial Growth at the Colonic Surface
Miller, B. M., Liou, M. J., Zhang, L. F., Nguyen, H., Litvak, Y., Schorr, E., Jang, K. K., Tiffany, C. R., Butler, B. P., & Bäumler, A. J. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.10.009 · Cited by 71 · see citing works
“By supplying the habitat, the host wields a prominent influence over microbial growth at body surfaces (Byndloss et al., 2018; Foster et al., 2017).”
Background
Longitudinal Microbiome Composition and Stability Correlate with Increased Weight and Length of Very-Low-Birth-Weight Infants
Yee, A. L., Miller, E. M., Dishaw, L. J., Gordon, J. M., Ji, M., Dutra, S. V. O., Ho, T. T. B., Gilbert, J. A., & Groer, M. E. (2019) · mSystems · doi:10.1128/msystems.00229-18 · Cited by 68 · see citing works
Impact of the mother's gut microbiota on infant microbiome and brain development
Mady, E. A., Doghish, A. S., El‐Dakroury, W. A., Elkhawaga, S. Y., Ismail, A., El‐Mahdy, H. A., Elsakka, E. G. E., & El‐Husseiny, H. M. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105195 · Cited by 69 · see citing works
Beneficial effects of seaweed-derived dietary fiber: Highlights of the sulfated polysaccharides
Huang, W., Tan, H., & Nie, S. (2021) · Food Chemistry · doi:10.1016/j.foodchem.2021.131608 · Cited by 69 · see citing works
Dual functional roles of the MyD88 signaling in colorectal cancer development
Wang, L., Yu, K., Zhang, X., & Yu, S. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.07.139 · Cited by 61 · see citing works
The human gut microbiome in health and disease: time for a new chapter?
Lee, J., Bays, D. J., Savage, H. P., & Bäumler, A. J. (2024) · Infection and Immunity · doi:10.1128/iai.00302-24 · Cited by 58 · see citing works
“The resulting shift from an anoxic to an oxic environment sets the stage for colonic domination by facultatively anaerobic microorganisms (75–77, 101–103) (Fig.”
Gastrointestinal host-pathogen interaction in the age of microbiome research
Tsolis, R. M., & Bäumler, A. J. (2020) · Current Opinion in Microbiology · doi:10.1016/j.mib.2020.03.002 · Cited by 53 · see citing works
Assessment of clinical and microbiota responses to fecal microbial transplantation in adult horses with diarrhea
McKinney, C. A., Bedenice, D., PACHECO, A. P. D. S., Oliveira, B. C. M., Paradis, M. R., Mazan, M. R., & Widmer, G. (2021) · PLoS ONE · doi:10.1371/journal.pone.0244381 · Cited by 52 · see citing works
“Of particular interest would be to examine whether WCHB-1 abundance promotes recovery from colitis or is simply a consequence of the re-establishment of anaerobic conditions following an episode of diarrhea [52].”
Background
Synthetic gut microbiome: Advances and challenges
Mabwi, H. A., Kim, E., Song, D., Yoon, H. S., Pan, C., Komba, E. V. G., Ko, G., & Cha, K. H. (2020) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2020.12.029 · Cited by 51 · see citing works
“As these variations include immunological differences, transit time, intestinal structure, and functional caecum presence [58,59], cur-”
Background
Multiomics analysis of soybean meal induced marine fish enteritis in juvenile pearl gentian grouper, Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂
Zhang, W., Tan, B., Deng, J., & Zhang, H. (2021) · Scientific Reports · doi:10.1038/s41598-021-02278-z · Cited by 50 · see citing works
Microbial Control of Intestinal Homeostasis via Enteroendocrine Cell Innate Immune Signaling
Watnick, P. I., & Jugder, B. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2019.09.005 · Cited by 49 · see citing works
At the right time in the right place: How do luminal gradients position the microbiota along the gut?
Chikina, A. S., & Vignjevic, D. M. (2021) · Cells and Development · doi:10.1016/j.cdev.2021.203712 · Cited by 48 · see citing works
The Klebsiella pneumoniae citrate synthase gene, gltA, influences site specific fitness during infection
Sun, Y., Vornhagen, J., Breen, P. A., Forsyth, V. S., Zhao, L., Mobley, H. L. T., & Bachman, M. A. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1008010 · Cited by 43 · see citing works
Modulation of the gut microbiota to improve innate resistance
Schnupf, P., Gaboriau‐Routhiau, V., & Cerf–Bensussan, N. (2018) · Current Opinion in Immunology · doi:10.1016/j.coi.2018.08.003 · Cited by 46 · see citing works
Microbiota-Nourishing Immunity: A Guide to Understanding Our Microbial Self
Litvak, Y., & Bäumler, A. J. (2019) · Immunity · doi:10.1016/j.immuni.2019.08.003 · Cited by 43 · see citing works
Ambient oxygen levels regulate intestinal dysbiosis and GVHD severity after allogeneic stem cell transplantation
Seike, K., Kiledal, E. A., Fujiwara, H., Henig, I. J., da Silva, M. B., van den Brink, M. R. M., Hein, R., Hoostal, M. J., Liu, C., Oravecz-Wilson, K. I., et al. (2023) · Immunity · doi:10.1016/j.immuni.2023.01.007 · Cited by 42 · see citing works
Innate lymphoid cell type 3–derived interleukin-22 boosts lipocalin-2 production in intestinal epithelial cells via synergy between STAT3 and NF-κB
Coorens, M., Rao, A., Gräfe, S. K., Unelius, D., Lindforss, U., Agerberth, B., Mjösberg, J., & Bergman, P. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.007290 · Cited by 39 · see citing works
“Enterobacteriaceae is a large family of Gram-negative bacteria that are commonly found as part of the human intestinal microbiota and include species such as Escherichia coli and Klebsiella pneumoniae (1, 2).”
Background
The longitudinal and cross-sectional heterogeneity of the intestinal microbiota
Miller, B. M., Liou, M. J., Lee, J., & Bäumler, A. J. (2021) · Current Opinion in Microbiology · doi:10.1016/j.mib.2021.08.004 · Cited by 38 · see citing works
Lactobacillus rhamnosus and L. plantarum Combination Treatment Ameliorated Colitis Symptoms in a Mouse Model by Altering Intestinal Microbial Composition and Suppressing Inflammatory Response
Liu, Y., Zhang, H., Xie, A., Sun, J., Yang, H., Li, J., Li, Y., Chen, F., Mei, Y., & Liang, Y. (2023) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202200340 · Cited by 36 · see citing works
Integrating research on bacterial pathogens and commensals to fight infections—an ecological perspective
Maier, L., Stein‐Thoeringer, C. K., Ley, R. E., Brötz‐Oesterhelt, H., Link, H., Ziemert, N., Wagner, S., & Peschel, A. (2024) · The Lancet Microbe · doi:10.1016/s2666-5247(24)00049-1 · Cited by 36 · see citing works
Colonization resistance against multi-drug-resistant bacteria: a narrative review
Guern, R. L., Stabler, S., Gosset, P., Pichavant, M., Grandjean, T., Faure, E., Karaca, Y., Faure, K., Kipnis, É., & Dessein, R. (2021) · Journal of Hospital Infection · doi:10.1016/j.jhin.2021.09.001 · Cited by 37 · see citing works
Safety assessment of monosodium glutamate based on intestinal function and flora in mice
Xu, J., Tang, M., Liu, Y., Xu, J., & Xu, X. (2021) · Food Science and Human Wellness · doi:10.1016/j.fshw.2021.07.016 · Cited by 36 · see citing works
Mechanisms underlying alterations of the gut microbiota by exercise and their role in shaping ecological resilience
Mohr, A. E., Mach, N., Pugh, J. N., Grosicki, G. J., Allen, J. M., Karl, J. P., & Whisner, C. M. (2025) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaf037 · Cited by 34 · see citing works
“Ecologically, diet exerts strong selective pressures on gut microbial communities (Byndloss et al. 2018 ), driven by competition for nutrients and increased fitness through cross-feeding interactions (Morris et al. 2013 ).”
Microbiota-nourishing Immunity and Its Relevance for Ulcerative Colitis
Byndloss, M. X., Litvak, Y., & Bäumler, A. J. (2019) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izz004 · Cited by 33 · see citing works
The Habitat Filters of Microbiota-Nourishing Immunity
Miller, B. M., & Bäumler, A. J. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101819-024945 · Cited by 32 · see citing works
Effects of combination treatment with metformin and berberine on hypoglycemic activity and gut microbiota modulation in db/db mice
Lyu, Y., Li, D. X., Yuan, X., Li, Z., Zhang, J., Ming, X., Shaw, P. C., Zhang, C., Kong, A. P. S., & Zuo, Z. (2022) · Phytomedicine · doi:10.1016/j.phymed.2022.154099 · Cited by 31 · see citing works
Contributors to Dysbiosis in Very-Low-Birth-Weight Infants
Groer, M. E., Miller, E. M., D’Agata, A. L., Ho, T. T. B., Dutra, S. V. O., Yoo, J. Y., Yee, A. L., Gilbert, J. A., & Dishaw, L. J. (2020) · Journal of Obstetric, Gynecologic & Neonatal Nursing · doi:10.1016/j.jogn.2020.02.003 · Cited by 30 · see citing works
The Metallome as a Link Between the “Omes” in Autism Spectrum Disorders
Stanton, J. E., Malijauskaite, S., McGourty, K., & Grabrucker, A. M. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.695873 · Cited by 16 · see citing works
Enabling oxygen-controlled microfluidic cultures for spatiotemporal microbial single-cell analysis
Kasahara, K., Leygeber, M., Seiffarth, J., Ruzaeva, K., Drepper, T., Nöh, K., & Kohlheyer, D. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1198170 · Cited by 17 · see citing works
Unbalanced diets enhance the complexity of gut microbial network but destabilize its stability and resistance
Sun, P., Wang, M., Zheng, W., Li, S., Zhu, X., Chai, X., & Zhao, S. (2023) · Stress Biology · doi:10.1007/s44154-023-00098-x · Cited by 17 · see citing works
“In ecological terms, diet habit is one of the most important selection pressures on the gut microbiota, partly caused by competition for nutrients (Byndloss et al. 2018).”
Background
Paneth cells: Maintaining dynamic microbiome‐host homeostasis, protecting against inflammation and cancer
Nikolenko, V. N., Oganesyan, M. V., Sankova, M. V., Bulygin, K. V., Vovkogon, A. D., Rizaeva, N. A., & Sinelnikov, M. Y. (2020) · BioEssays · doi:10.1002/bies.202000180 · Cited by 17 · see citing works
Tackling the Threat of Cancer Due to Pathobionts Producing Colibactin: Is Mesalamine the Magic Bullet?
Tang-Fichaux, M., Branchu, P., Nougayrède, J., & Oswald, É. (2021) · Toxins · doi:10.3390/toxins13120897 · Cited by 16 · see citing works
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Authors: Byndloss, M. X., Pernitzsch, S. R., & Bäumler, A. J.
Affiliations: University of California, Davis (US)
Corresponding author: Bäumler, Andreas J.
ORCID: Byndloss, Mariana X.
Pernitzsch, Sandy R.
Bäumler, Andreas J.
Venue: Mucosal Immunology
Publisher: Elsevier BV
Published: 2018-09
Volume: 11
Issue: 5
Pages: 1299-1305
ISSN: 1933-0219 (ISSN-L)
DOI: 10.1038/s41385-018-0010-y
OpenAlex: W2800529903
Cited by: 109
References: 106
Citations by year: 2026: 4 · 2025: 11 · 2024: 17 · 2023: 13 · 2022: 8 · 2021: 20 · 2020: 16 · 2019: 16 · 2018: 4
FWCI: 1.37
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 1244 d)
Locations: Mucosal Immunology (publishedVersion)
PubMed (publishedVersion)
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 › Animal Science and Zoology › Animal Nutrition and Physiology
Keywords: gut microbiota, host-microbe interactions, microbial homeostasis, Paneth cells, antimicrobial peptides, dietary fiber fermentation, small intestine, large intestine, dysbiosis
MeSH terms: Gastrointestinal Microbiome, Host Microbial Interactions, Animals, Ecology, Epithelial Cells, Homeostasis, Humans, Intestinal Mucosa, Intestines, Microbiota

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Healthy hosts rule within: ecological forces shaping the gut microbiota

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