In Silico Analysis of the Small Molecule Content of Outer Membrane Vesicles Produced by Bacteroides thetaiotaomicron Indicates an Extensive Metabolic Link between Microbe and Host
The interactions between the gut microbiota and its host are of central importance to the health of the host. Outer membrane vesicles (OMVs) are produced ubiquitously by Gram-negative bacteria including the gut commensal Bacteroides thetaiotaomicron. These vesicles can interact with the host in vari...
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| Format: | Article |
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Frontiers Media S.A.
2017-12-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2017.02440/full |
| _version_ | 1831839438383087616 |
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| author | William A. Bryant Régis Stentz Gwenaelle Le Gall Michael J. E. Sternberg Simon R. Carding Simon R. Carding Thomas Wilhelm |
| author_facet | William A. Bryant Régis Stentz Gwenaelle Le Gall Michael J. E. Sternberg Simon R. Carding Simon R. Carding Thomas Wilhelm |
| author_sort | William A. Bryant |
| collection | DOAJ |
| description | The interactions between the gut microbiota and its host are of central importance to the health of the host. Outer membrane vesicles (OMVs) are produced ubiquitously by Gram-negative bacteria including the gut commensal Bacteroides thetaiotaomicron. These vesicles can interact with the host in various ways but until now their complement of small molecules has not been investigated in this context. Using an untargeted high-coverage metabolomic approach we have measured the small molecule content of these vesicles in contrasting in vitro conditions to establish what role these metabolites could perform when packed into these vesicles. B. thetaiotaomicron packs OMVs with a highly conserved core set of small molecules which are strikingly enriched with mouse-digestible metabolites and with metabolites previously shown to be associated with colonization of the murine GIT. By use of an expanded genome-scale metabolic model of B. thetaiotaomicron and a potential host (the mouse) we have established many possible metabolic pathways between the two organisms that were previously unknown, and have found several putative novel metabolic functions for mouse that are supported by gene annotations, but that do not currently appear in existing mouse metabolic networks. The lipidome of these OMVs bears no relation to the mouse lipidome, so the purpose of this particular composition of lipids remains unclear. We conclude from this analysis that through intimate symbiotic evolution OMVs produced by B. thetaiotaomicron are likely to have been adopted as a conduit for small molecules bound for the mammalian host in vivo. |
| first_indexed | 2024-12-23T05:53:16Z |
| format | Article |
| id | doaj.art-9d4359788872456090e0abdf50873756 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-23T05:53:16Z |
| publishDate | 2017-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-9d4359788872456090e0abdf508737562022-12-21T17:57:54ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-12-01810.3389/fmicb.2017.02440299488In Silico Analysis of the Small Molecule Content of Outer Membrane Vesicles Produced by Bacteroides thetaiotaomicron Indicates an Extensive Metabolic Link between Microbe and HostWilliam A. Bryant0Régis Stentz1Gwenaelle Le Gall2Michael J. E. Sternberg3Simon R. Carding4Simon R. Carding5Thomas Wilhelm6Centre for Integrative Systems Biology and Bioinformatics, Department of Life Sciences, Imperial College London, London, United KingdomGut Health and Food Safety Programme, Quadram Institute Bioscience, Norwich, United KingdomMetabolomics Unit, Quadram Institute Bioscience, Norwich, United KingdomCentre for Integrative Systems Biology and Bioinformatics, Department of Life Sciences, Imperial College London, London, United KingdomGut Health and Food Safety Programme, Quadram Institute Bioscience, Norwich, United KingdomNorwich Medical School, University of East Anglia, Norwich, United KingdomTheoretical Systems Biology Lab, Quadram Institute Bioscience, Norwich, United KingdomThe interactions between the gut microbiota and its host are of central importance to the health of the host. Outer membrane vesicles (OMVs) are produced ubiquitously by Gram-negative bacteria including the gut commensal Bacteroides thetaiotaomicron. These vesicles can interact with the host in various ways but until now their complement of small molecules has not been investigated in this context. Using an untargeted high-coverage metabolomic approach we have measured the small molecule content of these vesicles in contrasting in vitro conditions to establish what role these metabolites could perform when packed into these vesicles. B. thetaiotaomicron packs OMVs with a highly conserved core set of small molecules which are strikingly enriched with mouse-digestible metabolites and with metabolites previously shown to be associated with colonization of the murine GIT. By use of an expanded genome-scale metabolic model of B. thetaiotaomicron and a potential host (the mouse) we have established many possible metabolic pathways between the two organisms that were previously unknown, and have found several putative novel metabolic functions for mouse that are supported by gene annotations, but that do not currently appear in existing mouse metabolic networks. The lipidome of these OMVs bears no relation to the mouse lipidome, so the purpose of this particular composition of lipids remains unclear. We conclude from this analysis that through intimate symbiotic evolution OMVs produced by B. thetaiotaomicron are likely to have been adopted as a conduit for small molecules bound for the mammalian host in vivo.http://journal.frontiersin.org/article/10.3389/fmicb.2017.02440/fullBacteroides thetaiotaomicron VPI-5482outer membrane vesiclemetabolomicsgenome-scale metabolic modelinghost–microbe interaction |
| spellingShingle | William A. Bryant Régis Stentz Gwenaelle Le Gall Michael J. E. Sternberg Simon R. Carding Simon R. Carding Thomas Wilhelm In Silico Analysis of the Small Molecule Content of Outer Membrane Vesicles Produced by Bacteroides thetaiotaomicron Indicates an Extensive Metabolic Link between Microbe and Host Frontiers in Microbiology Bacteroides thetaiotaomicron VPI-5482 outer membrane vesicle metabolomics genome-scale metabolic modeling host–microbe interaction |
| title | In Silico Analysis of the Small Molecule Content of Outer Membrane Vesicles Produced by Bacteroides thetaiotaomicron Indicates an Extensive Metabolic Link between Microbe and Host |
| title_full | In Silico Analysis of the Small Molecule Content of Outer Membrane Vesicles Produced by Bacteroides thetaiotaomicron Indicates an Extensive Metabolic Link between Microbe and Host |
| title_fullStr | In Silico Analysis of the Small Molecule Content of Outer Membrane Vesicles Produced by Bacteroides thetaiotaomicron Indicates an Extensive Metabolic Link between Microbe and Host |
| title_full_unstemmed | In Silico Analysis of the Small Molecule Content of Outer Membrane Vesicles Produced by Bacteroides thetaiotaomicron Indicates an Extensive Metabolic Link between Microbe and Host |
| title_short | In Silico Analysis of the Small Molecule Content of Outer Membrane Vesicles Produced by Bacteroides thetaiotaomicron Indicates an Extensive Metabolic Link between Microbe and Host |
| title_sort | in silico analysis of the small molecule content of outer membrane vesicles produced by bacteroides thetaiotaomicron indicates an extensive metabolic link between microbe and host |
| topic | Bacteroides thetaiotaomicron VPI-5482 outer membrane vesicle metabolomics genome-scale metabolic modeling host–microbe interaction |
| url | http://journal.frontiersin.org/article/10.3389/fmicb.2017.02440/full |
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