Regulation of host weight gain and lipid metabolism by bacterial bile acid modification in the gut
Open accessAbstract
Significance: It is known that the gastrointestinal microbiota influences adiposity and weight gain in the host. However the mechanisms by which gut microorganisms coordinate host physiological processes are currently unclear. We demonstrate that a single, widely distributed function of the gut microbiota, bile salt hydrolase (BSH) activity, significantly influences lipid metabolism, weight gain, and cholesterol levels in the host. In our study microbial BSH activity was shown to direct expression of host signalling pathways with known roles in lipid metabolism, circadian rhythm, and epithelial cell function. The work defines the significant impact of in situ bile hydrolysis on host metabolism and indicates how this finding may be exploited as a potential intervention strategy for the control of obesity and metabolic syndrome.
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By activating FXR signaling, bile acids induce expression of anti-microbial defense genes (iNOS and RegIIIγ) protecting the gut from epithelial deterioration and bacterial translocation.
“Furthermore, by activating FXR signaling, bile acids can induce the expression of anti-microbial defense genes in the host (such as the inducible isoform of nitric oxide synthases -iNOS, and the antibacterial lectin -RegIIIγ) protecting the gut from epithelial deterioration and bacterial translocation (Inagaki et al., 2006;Joyce et al., 2014).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Joyce et al., 2014
AHR is activated by both bacterially conjugated and conventional bile acids in vitro.
“We previously showed that Glu-conjugated bile acids were activators of human PXR in vitro14, and herein, we observed activation of AHR by both bacterially conjugated and conventional bile acids in vitro.”
From Bile Acids Are Substrates for Amine N-Acyl Transferase Activity by Bile Salt Hydrolase (2022) · cites this paper as [14]
Bacterial BSH activity affects systemic metabolic processes and adiposity in the host.
“Bacterial BSH activity affects systemic metabolic processes and adiposity in the host.”
Bacterial BSH activity represents a key mechanistic target for the control of obesity and hypercholesterolemia, acting by deconjugating bile acids to generate unconjugated bile acids.
“It also represents a key mechanistic target for the control of obesity and hypercholesterolemia, acting by deconjugating BAs to generate unconjugated BAs (42).”
BAs are toxic for many bacterial species and induce the expression of anti-microbial defense genes in the host (including iNOS, RegIIIγ).
“BAs are toxic for many bacterial species; they also induce the expression of anti-microbial defense genes in the host (including iNOS, RegIIIγ) (Inagaki et al., 2006; Joyce et al., 2014).”
From Microbiota-related Changes in Bile Acid & Tryptophan Metabolism are Associated with Gastrointestinal Dysfunction in a Mouse Model of Autism (2017) · cites this paper as Joyce et al., 2014
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Ryan, P. M., London, L. E. E., Bjorndahl, T. C., Mandal, R., Murphy, K., Fitzgerald, G. F., Shanahan, F., Ross, R. P., Wishart, D. S., Caplice, N. M., et al. (2017) · Microbiome · doi:10.1186/s40168-017-0246-x · Cited by 97 · see citing works
Self-citationAgolino, G., Pino, A., Vaccalluzzo, A., Cristofolini, M., Solieri, L., Caggia, C., & Randazzo, C. L. (2024) · Journal of Functional Foods · doi:10.1016/j.jff.2024.106357 · Cited by 87 · see citing works
O’Donovan, S. M., Crowley, E. K., Brown, J. R. ‐., O’Sullivan, O., O’Leary, O. F., Timmons, S., Nolan, Y. M., Clarke, D. J., Hyland, N. P., Joyce, S. A., et al. (2020) · Neurogastroenterology & Motility · doi:10.1111/nmo.13726 · Cited by 86 · see citing works
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The influence of probiotics on bile acids in diseases and aging
Sivamaruthi, B. S., Fern, L. A., Rashidah Pg Hj Ismail, D. S. N., & Chaiyasut, C. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110310 · Cited by 73 · see citing works
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New insights into microbial bile salt hydrolases: from physiological roles to potential applications
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Functional and Phylogenetic Diversity of BSH and PVA Enzymes
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Self-citationFunctional food addressing heart health: do we have to target the gut microbiota?
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“Recently, several studies have underscored the pivotal role of BSH in lipid metabolism and in mediating host–microbe interactions [67–69].”
- Authors
- Joyce, S. A., MacSharry, J., Casey, P. G., Kinsella, M., Murphy, E. F., Shanahan, F., Hill, C., & Gahan, C. G. M.
- Affiliations
- APC Microbiome Institute (IE)
- Nutrition, and
- University College Cork (IE)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-05-05
- Volume
- 111
- Issue
- 20
- Pages
- 7421-7426
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4034235
- OpenAlex
- W1966311917
- Cited by
- 604
- References
- 40
- Citations by year
- 2026: 45 · 2025: 50 · 2024: 51 · 2023: 44 · 2022: 61 · 2021: 60 · 2020: 70 · 2019: 50 · 2018: 49 · 2017: 39 · 2016: 39 · 2015: 35 · 2014: 11
- FWCI
- 16.94
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
- Keywords
- gut microbiota, obesity, lipid metabolism, cholesterol metabolism, bile acids, host energy metabolism, adiposity, gnotobiotic mice, microbial gene function, PPARγ, ABCG5/8, RegIIIγ, circadian rhythm, hypercholesterolemia, weight gain
- MeSH terms
- Animals, Bile Acids and Salts, Circadian Rhythm, Escherichia coli, Germ-Free Life, Hydrolysis, Lactobacillus, Male, Mice, Inbred C57BL, Transcription, Genetic, Signal Transduction, Weight Gain, Metabolic Syndrome, Gastrointestinal Tract, Adiposity, Lipid Metabolism, Mice, Adiponectin
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