Reverse metabolomics for the discovery of chemical structures from humans
Determining the structure and phenotypic context of molecules detected in untargeted metabolomics experiments remains challenging. Here we present reverse metabolomics as a discovery strategy, whereby tandem mass spectrometry spectra acquired from newly synthesized compounds are searched for in publ...
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| Published in | Nature (London) Vol. 626; no. 7998; pp. 419 - 426 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
08.02.2024
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Determining the structure and phenotypic context of molecules detected in untargeted metabolomics experiments remains challenging. Here we present reverse metabolomics as a discovery strategy, whereby tandem mass spectrometry spectra acquired from newly synthesized compounds are searched for in public metabolomics datasets to uncover phenotypic associations. To demonstrate the concept, we broadly synthesized and explored multiple classes of metabolites in humans, including
N
-acyl amides, fatty acid esters of hydroxy fatty acids, bile acid esters and conjugated bile acids. Using repository-scale analysis
1
,
2
, we discovered that some conjugated bile acids are associated with inflammatory bowel disease (IBD). Validation using four distinct human IBD cohorts showed that cholic acids conjugated to Glu, Ile/Leu, Phe, Thr, Trp or Tyr are increased in Crohn’s disease. Several of these compounds and related structures affected pathways associated with IBD, such as interferon-γ production in CD4
+
T cells
3
and agonism of the pregnane X receptor
4
. Culture of bacteria belonging to the
Bifidobacterium
,
Clostridium
and
Enterococcus
genera produced these bile amidates. Because searching repositories with tandem mass spectrometry spectra has only recently become possible, this reverse metabolomics approach can now be used as a general strategy to discover other molecules from human and animal ecosystems.
A new discovery strategy, ‘reverse metabolomics’, facilitates high-throughput matching of mass spectrometry spectra in public untargeted metabolomics datasets, and a proof-of-concept experiment identified an association between microbial bile amidates and inflammatory bowel disease. |
|---|---|
| AbstractList | Determining the structure and phenotypic context of molecules detected in untargeted metabolomics experiments remains challenging. Here we present reverse metabolomics as a discovery strategy, whereby tandem mass spectrometry spectra acquired from newly synthesized compounds are searched for in public metabolomics datasets to uncover phenotypic associations. To demonstrate the concept, we broadly synthesized and explored multiple classes of metabolites in humans, including N -acyl amides, fatty acid esters of hydroxy fatty acids, bile acid esters and conjugated bile acids. Using repository-scale analysis 1,2 , we discovered that some conjugated bile acids are associated with inflammatory bowel disease (IBD). Validation using four distinct human IBD cohorts showed that cholic acids conjugated to Glu, Ile/Leu, Phe, Thr, Trp or Tyr are increased in Crohn’s disease. Several of these compounds and related structures affected pathways associated with IBD, such as interferon-γ production in CD4 + T cells 3 and agonism of the pregnane X receptor 4 . Culture of bacteria belonging to the Bifidobacterium , Clostridium and Enterococcus genera produced these bile amidates. Because searching repositories with tandem mass spectrometry spectra has only recently become possible, this reverse metabolomics approach can now be used as a general strategy to discover other molecules from human and animal ecosystems. Determining the structure and phenotypic context of molecules detected in untargeted metabolomics experiments remains challenging. Here we present reverse metabolomics as a discovery strategy, whereby tandem mass spectrometry spectra acquired from newly synthesized compounds are searched for in public metabolomics datasets to uncover phenotypic associations. To demonstrate the concept, we broadly synthesized and explored multiple classes of metabolites in humans, including /V-acyl amides, fatty acid esters of hydroxy fatty acids, bile acid esters and conjugated bile acids. Using repository-scale analysis1-2, we discovered that some conjugated bile acids are associated with inflammatory bowel disease (1BD). Validation using four distinct human 1BD cohorts showed that cholic acids conjugated to Glu, lle/Leu, Phe, Thr, Trp or Tyr are increased in Crohn's disease. Several of these compounds and related structures affected pathways associated with 1BD, such as interferon-y production in CD4+T cells3 and agonism of the pregnane X receptor4. Culture of bacteria belonging to the B,fidobacterium, Clostridium and Enterococcus genera produced these bile amidates. Because searching repositories with tandem mass spectrometry spectra has only recently become possible, this reverse metabolomics approach can now be used as a general strategy to discover other molecules from human and animal ecosystems. Determining the structure and phenotypic context of molecules detected in untargeted metabolomics experiments remains challenging. Here we present reverse metabolomics as a discovery strategy, whereby tandem mass spectrometry spectra acquired from newly synthesized compounds are searched for in public metabolomics datasets to uncover phenotypic associations. To demonstrate the concept, we broadly synthesized and explored multiple classes of metabolites in humans, including N -acyl amides, fatty acid esters of hydroxy fatty acids, bile acid esters and conjugated bile acids. Using repository-scale analysis 1 , 2 , we discovered that some conjugated bile acids are associated with inflammatory bowel disease (IBD). Validation using four distinct human IBD cohorts showed that cholic acids conjugated to Glu, Ile/Leu, Phe, Thr, Trp or Tyr are increased in Crohn’s disease. Several of these compounds and related structures affected pathways associated with IBD, such as interferon-γ production in CD4 + T cells 3 and agonism of the pregnane X receptor 4 . Culture of bacteria belonging to the Bifidobacterium , Clostridium and Enterococcus genera produced these bile amidates. Because searching repositories with tandem mass spectrometry spectra has only recently become possible, this reverse metabolomics approach can now be used as a general strategy to discover other molecules from human and animal ecosystems. A new discovery strategy, ‘reverse metabolomics’, facilitates high-throughput matching of mass spectrometry spectra in public untargeted metabolomics datasets, and a proof-of-concept experiment identified an association between microbial bile amidates and inflammatory bowel disease. Determining the structure and phenotypic context of molecules detected in untargeted metabolomics experiments remains challenging. Here we present reverse metabolomics as a discovery strategy, whereby tandem mass spectrometry spectra acquired from newly synthesized compounds are searched for in public metabolomics datasets to uncover phenotypic associations. To demonstrate the concept, we broadly synthesized and explored multiple classes of metabolites in humans, including N-acyl amides, fatty acid esters of hydroxy fatty acids, bile acid esters and conjugated bile acids. Using repository-scale analysis1,2, we discovered that some conjugated bile acids are associated with inflammatory bowel disease (IBD). Validation using four distinct human IBD cohorts showed that cholic acids conjugated to Glu, Ile/Leu, Phe, Thr, Trp or Tyr are increased in Crohn's disease. Several of these compounds and related structures affected pathways associated with IBD, such as interferon-γ production in CD4+ T cells3 and agonism of the pregnane X receptor4. Culture of bacteria belonging to the Bifidobacterium, Clostridium and Enterococcus genera produced these bile amidates. Because searching repositories with tandem mass spectrometry spectra has only recently become possible, this reverse metabolomics approach can now be used as a general strategy to discover other molecules from human and animal ecosystems.Determining the structure and phenotypic context of molecules detected in untargeted metabolomics experiments remains challenging. Here we present reverse metabolomics as a discovery strategy, whereby tandem mass spectrometry spectra acquired from newly synthesized compounds are searched for in public metabolomics datasets to uncover phenotypic associations. To demonstrate the concept, we broadly synthesized and explored multiple classes of metabolites in humans, including N-acyl amides, fatty acid esters of hydroxy fatty acids, bile acid esters and conjugated bile acids. Using repository-scale analysis1,2, we discovered that some conjugated bile acids are associated with inflammatory bowel disease (IBD). Validation using four distinct human IBD cohorts showed that cholic acids conjugated to Glu, Ile/Leu, Phe, Thr, Trp or Tyr are increased in Crohn's disease. Several of these compounds and related structures affected pathways associated with IBD, such as interferon-γ production in CD4+ T cells3 and agonism of the pregnane X receptor4. Culture of bacteria belonging to the Bifidobacterium, Clostridium and Enterococcus genera produced these bile amidates. Because searching repositories with tandem mass spectrometry spectra has only recently become possible, this reverse metabolomics approach can now be used as a general strategy to discover other molecules from human and animal ecosystems. Determining the structure and phenotypic context of molecules detected in untargeted metabolomics experiments remains challenging. Here we present reverse metabolomics as a discovery strategy, whereby tandem mass spectrometry spectra acquired from newly synthesized compounds are searched for in public metabolomics datasets to uncover phenotypic associations. To demonstrate the concept, we broadly synthesized and explored multiple classes of metabolites in humans, including N-acyl amides, fatty acid esters of hydroxy fatty acids, bile acid esters and conjugated bile acids. Using repository-scale analysis , we discovered that some conjugated bile acids are associated with inflammatory bowel disease (IBD). Validation using four distinct human IBD cohorts showed that cholic acids conjugated to Glu, Ile/Leu, Phe, Thr, Trp or Tyr are increased in Crohn's disease. Several of these compounds and related structures affected pathways associated with IBD, such as interferon-γ production in CD4 T cells and agonism of the pregnane X receptor . Culture of bacteria belonging to the Bifidobacterium, Clostridium and Enterococcus genera produced these bile amidates. Because searching repositories with tandem mass spectrometry spectra has only recently become possible, this reverse metabolomics approach can now be used as a general strategy to discover other molecules from human and animal ecosystems. |
| Author | Zuffa, Simone Yan, Tingting Avila-Pacheco, Julian Lu, Hsueh-han Clish, Clary B. Baker, Erin S. Knight, Rob Patterson, Andrew D. Hao, Fuhua Stewart, Allison K. Plichta, Damian R. Gentry, Emily C. Belda-Ferre, Pedro Chu, Hiutung Siegel, Dionicio Boland, Brigid S. Vande Casteele, Niels Collins, Stephanie L. Dorrestein, Pieter C. Ananthakrishnan, Ashwin N. Carrillo Terrazas, Marvic Jarmusch, Alan K. Aron, Allegra T. Hemperly, Amy Syrkin-Nikolau, Mashette Gonzalez, Frank J. Xavier, Ramnik J. Wang, Mingxun Panitchpakdi, Morgan Vlamakis, Hera |
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Belda-Ferre fullname: Belda-Ferre, Pedro organization: Department of Pediatrics, University of California, San Diego, Department of Computer Science and Engineering, Jacobs School of Engineering, University of California, San Diego – sequence: 5 givenname: Allison K. surname: Stewart fullname: Stewart, Allison K. organization: Department of Chemistry, North Carolina State University – sequence: 6 givenname: Marvic surname: Carrillo Terrazas fullname: Carrillo Terrazas, Marvic organization: Department of Pathology, University of California, San Diego – sequence: 7 givenname: Hsueh-han orcidid: 0000-0002-0832-9607 surname: Lu fullname: Lu, Hsueh-han organization: Department of Pathology, University of California, San Diego – sequence: 8 givenname: Simone surname: Zuffa fullname: Zuffa, Simone organization: Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego – sequence: 9 givenname: Tingting surname: Yan fullname: Yan, Tingting organization: Laboratory of Metabolism, Center for Cancer Research, National Cancer Institute, National Institutes of Health – sequence: 10 givenname: Julian orcidid: 0000-0001-9388-3946 surname: Avila-Pacheco fullname: Avila-Pacheco, Julian organization: Broad Institute of MIT and Harvard – sequence: 11 givenname: Damian R. orcidid: 0000-0002-6555-2557 surname: Plichta fullname: Plichta, Damian R. organization: Broad Institute of MIT and Harvard – sequence: 12 givenname: Allegra T. surname: Aron fullname: Aron, Allegra T. organization: Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego – sequence: 13 givenname: Mingxun orcidid: 0000-0001-7647-6097 surname: Wang fullname: Wang, Mingxun organization: Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego – sequence: 14 givenname: Alan K. orcidid: 0000-0002-2228-6308 surname: Jarmusch fullname: Jarmusch, Alan K. organization: Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, Immunity, Inflammation, and Disease Laboratory, Division of Intramural Research, National Institute of Environmental Health Sciences, National Institutes of Health – sequence: 15 givenname: Fuhua orcidid: 0000-0002-0865-5269 surname: Hao fullname: Hao, Fuhua organization: Center for Molecular Toxicology and Carcinogenesis, Department of Veterinary and Biomedical Sciences, The Pennsylvania State University – sequence: 16 givenname: Mashette surname: Syrkin-Nikolau fullname: Syrkin-Nikolau, Mashette organization: Division of Gastroenterology, Department of Pediatrics, Rady Children’s Hospital University of California San Diego – sequence: 17 givenname: Hera orcidid: 0000-0003-1086-9191 surname: Vlamakis fullname: Vlamakis, Hera organization: Broad Institute of MIT and Harvard, Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology – sequence: 18 givenname: Ashwin N. surname: Ananthakrishnan fullname: Ananthakrishnan, Ashwin N. organization: Division of Gastroenterology, Massachusetts General Hospital – sequence: 19 givenname: Brigid S. surname: Boland fullname: Boland, Brigid S. organization: Division of Gastroenterology, University of California, San Diego – sequence: 20 givenname: Amy surname: Hemperly fullname: Hemperly, Amy organization: Division of Gastroenterology, Department of Pediatrics, Rady Children’s Hospital University of California San Diego – sequence: 21 givenname: Niels surname: Vande Casteele fullname: Vande Casteele, Niels organization: Division of Gastroenterology, University of California, San Diego – sequence: 22 givenname: Frank J. orcidid: 0000-0002-7990-2140 surname: Gonzalez fullname: Gonzalez, Frank J. organization: Laboratory of Metabolism, Center for Cancer Research, National Cancer Institute, National Institutes of Health – sequence: 23 givenname: Clary B. orcidid: 0000-0001-8259-9245 surname: Clish fullname: Clish, Clary B. organization: Broad Institute of MIT and Harvard – sequence: 24 givenname: Ramnik J. orcidid: 0000-0002-5630-5167 surname: Xavier fullname: Xavier, Ramnik J. organization: Broad Institute of MIT and Harvard, Center for Microbiome Informatics and Therapeutics, Massachusetts Institute of Technology, Center for Computational and Integrative Biology, Massachusetts General Hospital and Harvard Medical School, Department of Molecular Biology, Massachusetts 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Computer Science and Engineering, Jacobs School of Engineering, University of California, San Diego, Center for Microbiome Innovation, Jacobs School of Engineering, University of California, San Diego, Department of Bioengineering, University of California, San Diego – sequence: 29 givenname: Dionicio surname: Siegel fullname: Siegel, Dionicio organization: Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego – sequence: 30 givenname: Pieter C. orcidid: 0000-0002-3003-1030 surname: Dorrestein fullname: Dorrestein, Pieter C. email: pdorrestein@health.ucsd.edu organization: Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38052229$$D View this record in MEDLINE/PubMed |
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| Copyright | The Author(s) 2023 2023. The Author(s). Copyright Nature Publishing Group Feb 8, 2024 |
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| Title | Reverse metabolomics for the discovery of chemical structures from humans |
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