Global chemical effects of the microbiome include new bile-acid conjugations
Open accessAbstract
A mosaic of cross-phylum chemical interactions occurs between all metazoans and their microbiomes. A number of molecular families that are known to be produced by the microbiome have a marked effect on the balance between health and disease 1-9. Considering the diversity of the human microbiome (which numbers over 40,000 operational taxonomic units 10), the effect of the microbiome on the chemistry of an entire animal remains underexplored. Here we use mass spectrometry informatics and data visualization approaches 11-13 to provide an assessment of the effects of the microbiome on the chemistry of an entire mammal by comparing metabolomics data from germ-free and specific-pathogen-free mice. We found that the microbiota affects the chemistry of all organs. This included the amino acid conjugations of host bile acids that were used to produce phenylalanocholic acid, tyrosocholic acid and leucocholic acid, which have not previously been characterized despite extensive research on bile-acid chemistry 14. These bile-acid conjugates were also found in humans, and were enriched in patients with inflammatory bowel disease or cystic fibrosis. These compounds agonized the farnesoid X receptor in vitro, and mice gavaged with the compounds showed reduced expression of bile-acid synthesis genes in vivo. Further studies are required to confirm whether these compounds have a physiological role in the host, and whether they contribute to gut diseases that are associated with microbiome dysbiosis.
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Some BBAAs activate host bile acid nuclear receptors like FXR and PXR.
“Some BBAAs activate host bile acid nuclear receptors like the farnesoid X receptor (FXR) and pregnane X receptor (PXR)1,3, but an assessment of other receptors has not been completed.”
From Bile Acids Are Substrates for Amine N-Acyl Transferase Activity by Bile Salt Hydrolase (2022) · cites this paper as [1]
The “Novel Bile Acids and FXR” section reports that phenylalanine- and tyrosine-conjugated bile acids activate human FXR in a cell-based assay. The passages in our copy do not report activation of PXR, so the citation supports the FXR part but not the PXR part. (LLM, conf=0.88)
Experimental — accuracy not yet measuredRecent studies demonstrated that bacteria have bile acid amine N-acyltransferase activity, with dozens of bacterially conjugated amino acid amidates identified.
“Recent studies demonstrated that bacteria, in addition to the host, have bile acid amine N-acyltransferase activity, with dozens of bacterially conjugated amino acid amidates identified1–4,6,17.”
From Bile Acids Are Substrates for Amine N-Acyl Transferase Activity by Bile Salt Hydrolase (2022) · cites this paper as [1]
In “Microbes produce the novel bile acids” (page unavailable), the paper reports that C. bolteae synthesized amino-acid-conjugated bile acids, supporting bacterial conjugation activity. In “Discovery of new conjugated bile acids” (page unavailable), it identifies three such amidates—phenylalanine, tyrosine, and leucine conjugates—not dozens. The cited paper therefore supports the bacterial activity but not the stated number of identified amidates. (LLM, conf=0.88)
Experimental — accuracy not yet measuredBSHs are gatekeepers of bile acid metabolism, capable of reshaping the BA landscape in the gut.
“The extensive compilation of recently identified MCBAs expands the complexity of the BSH-BA pool and reinforces BSHs as the gatekeepers of bile acid metabolism, capable of reshaping the BA landscape in the gut31,32.”
From Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut (2023) · cites this paper as [31]
The ‘Novel Bile Acids and FXR’ section identifies deconjugation as one mechanism of microbial bile-acid metabolism, supporting a role for microbial hydrolase activity in shaping bile acids. But it does not identify BSHs as gatekeepers: the enzyme responsible for the newly reported conjugations remains unknown, and ‘Discovery of new conjugated bile acids’ reports that those conjugates were not deconjugated in a human fecal culture. (LLM, conf=0.82)
Experimental — accuracy not yet measuredAn array of intestinal bacteria can catalyse the conjugation of BAs to a variety of amino acids through an unknown mechanism.
“An array of intestinal bacteria can catalyse the conjugation of BAs to a variety of amino acids through an unknown mechanism”
From Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut (2023) · cites this paper as [31]
In ‘Microbes produce the novel bile acids’ (page unavailable), two strains of one gut bacterial species, C. bolteae, synthesized phenylalanine- and tyrosine-conjugated bile acids. ‘Novel Bile Acids and FXR’ (page unavailable) also reports leucine conjugation associated with the microbiome and says the microbial enzyme remains unknown. The paper does not establish that an array of different intestinal bacteria can catalyse these conjugations. (LLM, conf=0.86)
Experimental — accuracy not yet measuredBSH enzymes can catalyse reconjugation to generate MCBAs capable of activating host ligand-activated receptors.
“Furthermore, BSH activity is complicated by the emerging data indicating that these enzymes can catalyse reconjugation to generate MCBAs capable of activating host ligand-activated receptors31,33,46,47.”
From Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut (2023) · cites this paper as [31]
The “Novel Bile Acids and FXR” section reports microbial reconjugation of bile acids and shows that the resulting conjugates activate human FXR in a cell-based assay. It explicitly says the microbial enzyme responsible remains unknown, so it does not support attributing reconjugation to BSH enzymes. No page number is available in our copy. (LLM, conf=0.90)
Experimental — accuracy not yet measured
Characterization data for all MCBAs are consistent with reported data.
“All MCBAs were purified according to literature precedent and characterization data are consistent with reported data31,33,42,77,78.”
From Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut (2023) · cites this paper as [31]
The Discovery of new conjugated bile acids section (page unavailable) reports retention-time and MS/MS matches between three bile acids and synthesized standards; Extended Data Fig. 5 shows those comparisons. The paper does not establish that characterization data for all MCBAs agree with previously reported data, or that all were purified according to literature precedent. (LLM, conf=0.78)
Experimental — accuracy not yet measuredCharacterization data for Glu-CDCA, Ile-CA, Leu-CA, Phe-CA, Trp-CDCA and Tyr-CA are consistent with reported data.
“Glu-CDCA, Ile-CA, Leu-CA, Phe-CA, Trp-CDCA and Tyr-CA were purified according to literature precedent and characterization data are consistent with reported data31,33.”
From Bile salt hydrolases shape the bile acid landscape and restrict Clostridioides difficile growth in the murine gut (2023) · cites this paper as [31]
The ‘Discovery of new conjugated bile acids’ section says Phe-CA, Tyr-CA and Leu-CA were validated against synthesized standards by retention time and MS/MS matching. Extended Data Fig. 5 also describes analysis of Ile-CA. Our copy does not provide corresponding characterization data for Glu-CDCA or Trp-CDCA, so it supports only part of the six-compound claim. (LLM, conf=0.86)
Experimental — accuracy not yet measuredBacteria in the gastrointestinal tract produce amino acid bile acid amidates that can affect host-mediated metabolic processes.
“Bacteria in the gastrointestinal tract produce amino acid bile acid amidates that can affect host-mediated metabolic processes1–6; however, the bacterial gene(s) responsible for their production remain unknown.”
From Bile Acids Are Substrates for Amine N-Acyl Transferase Activity by Bile Salt Hydrolase (2022) · cites this paper as [1]
The bacterial enzymes responsible for producing amino acid bile acid amidates are unknown.
“The enzymes responsible for these conjugation reactions are unknown.”
From Bile Acids Are Substrates for Amine N-Acyl Transferase Activity by Bile Salt Hydrolase (2022) · cites this paper as [1]
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Self-citation
- Authors
- Quinn, R. A., Melnik, A. V., Vrbanac, A., Fu, T., Patras, K. A., Christy, M. P., Bodai, Z., Belda-Ferre, P., Tripathi, A., Chung, L. K., Downes, M., Welch, R. D., Quinn, M., Humphrey, G., Panitchpakdi, M., Weldon, K. C., Aksenov, A., da Silva, R., Avila-Pacheco, J., Clish, C., Bae, S., Mallick, H., Franzosa, E. A., Lloyd-Price, J., Bussell, R., Thron, T., Nelson, A. T., Wang, M., Leszczynski, E., Vargas, F., Gauglitz, J. M., Meehan, M. J., Gentry, E., Arthur, T. D., Komor, A. C., Poulsen, O., Boland, B. S., Chang, J. T., Sandborn, W. J., Lim, M., Garg, N., Lumeng, J. C., Xavier, R. J., Kazmierczak, B. I., Jain, R., Egan, M., Rhee, K. E., Ferguson, D., Raffatellu, M., Vlamakis, H., Haddad, G. G., Siegel, D., Huttenhower, C., Mazmanian, S. K., Evans, R. M., Nizet, V., Knight, R., & Dorrestein, P. C.
- Affiliations
- University of California San Diego (US)
- Salk Institute for Biological Studies (US)
- Michigan State University (US)
- Broad Institute (US)
- Harvard University (US)
- California Institute of Technology (US)
- Georgia Institute of Technology (US)
- University of Michigan (US)
- Yale University (US)
- Corresponding author
- Dorrestein, Pieter C.
- ORCID
- Quinn, Robert A.
- Melnik, Alexey V.
- Vrbanac, Alison
- Patras, Kathryn A.
- Christy, Mitchell P.
- Bodai, Zsolt
- Tripathi, Anupriya
- Downes, Michael
- Quinn, Melissa
- Panitchpakdi, Morgan
- Weldon, Kelly C.
- Aksenov, Alexander
- Clish, Clary
- Mallick, Himel
- Franzosa, Eric A.
- Thron, Taren
- Nelson, Andrew T.
- Wang, Mingxun
- Leszczynski, Eric
- Vargas, Fernando
- Gauglitz, Julia M.
- Meehan, Michael J.
- Gentry, Emily
- Arthur, Timothy D.
- Komor, Alexis C.
- Boland, Brigid S.
- Chang, John T.
- Sandborn, William J.
- Garg, Neha
- Lumeng, Julie C.
- Xavier, Ramnik J.
- Kazmierczak, Barbara I.
- Jain, Ruchi
- Egan, Marie
- Rhee, Kyung E.
- Ferguson, David
- Raffatellu, Manuela
- Vlamakis, Hera
- Haddad, Gabriel G.
- Siegel, Dionicio
- Huttenhower, Curtis
- Mazmanian, Sarkis K.
- Evans, Ronald M.
- Nizet, Victor
- Knight, Rob
- Dorrestein, Pieter C.
- Venue
- Nature
- Published
- 2020-02-26
- Volume
- 579
- Issue
- 7797
- Pages
- 123-129
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7252668
- OpenAlex
- W3007415664
- Cited by
- 579
- References
- 43
- Citations by year
- 2026: 79 · 2025: 99 · 2024: 124 · 2023: 73 · 2022: 99 · 2021: 64 · 2020: 40
- FWCI
- 22.39
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (acceptedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Crohn's and Colitis Foundation (675191, 815985)
- National Institutes of Health (1s10rr029121-01, 1r03ca211211-01, KL2TR001444, UL1TR001863)
- National Heart, Lung, and Blood Institute (R01HL105278, R01HL116235, P01HL088093)
- National Cancer Institute (CA014195, R03 CA211211, P30CA014195)
- National Institute of General Medical Sciences (R01GM107550)
- National Institute of Allergy and Infectious Diseases (R01AI126277, U01AI124316)
- National Institute of Diabetes and Digestive and Kidney Diseases (R37DK057978, T32DK007494, R01DK057978, R24DK110499, P30DK120515, P30DK043351, P30DK040561)
- National Institute of Environmental Health Sciences (P42ES010337)
- National Institute of Dental and Craniofacial Research (U54DE023798)
- U.S. National Library of Medicine (T15LM011271)
- National Center for Research Resources (S10-RR029121)
- National Center for Advancing Translational Sciences
- National Center for Complementary and Integrative Health (DP1AT010885)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD084163)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Keywords
- gut microbiota, bile acid conjugation, farnesoid X receptor, germ-free mice, inflammatory bowel disease, cystic fibrosis, bile acid synthesis, dysbiosis, host metabolome
- MeSH terms
- Receptor, Farnesoid X-Activated, Animals, Bile Acids and Salts, Cystic Fibrosis, Germ-Free Life, Humans, Inflammatory Bowel Diseases, Receptors, Cytoplasmic and Nuclear, Cholic Acid, Mice, Metabolomics, Microbiota
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