Bioaccumulation of therapeutic drugs by human gut bacteria
Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. However, the systematic mapping of the interactions between drugs and bacteria has only started recently 1 and the main underlying mechanism proposed is the chemical transformation of drugs by microorganisms (biotra...
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| Veröffentlicht in: | Nature (London) Jg. 597; H. 7877; S. 533 - 538 |
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| Hauptverfasser: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Sprache: | Englisch |
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London
Nature Publishing Group UK
23.09.2021
Nature Publishing Group |
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| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
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| Abstract | Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. However, the systematic mapping of the interactions between drugs and bacteria has only started recently
1
and the main underlying mechanism proposed is the chemical transformation of drugs by microorganisms (biotransformation). Here we investigated the depletion of 15 structurally diverse drugs by 25 representative strains of gut bacteria. This revealed 70 bacteria–drug interactions, 29 of which had not to our knowledge been reported before. Over half of the new interactions can be ascribed to bioaccumulation; that is, bacteria storing the drug intracellularly without chemically modifying it, and in most cases without the growth of the bacteria being affected. As a case in point, we studied the molecular basis of bioaccumulation of the widely used antidepressant duloxetine by using click chemistry, thermal proteome profiling and metabolomics. We find that duloxetine binds to several metabolic enzymes and changes the metabolite secretion of the respective bacteria. When tested in a defined microbial community of accumulators and non-accumulators, duloxetine markedly altered the composition of the community through metabolic cross-feeding. We further validated our findings in an animal model, showing that bioaccumulating bacteria attenuate the behavioural response of
Caenorhabditis elegans
to duloxetine. Together, our results show that bioaccumulation by gut bacteria may be a common mechanism that alters drug availability and bacterial metabolism, with implications for microbiota composition, pharmacokinetics, side effects and drug responses, probably in an individual manner.
An analysis of the interactions between 15 drugs and 25 gut bacterial strains shows that bioaccumulation of drugs within bacterial cells is another mechanism through which gut microorganisms can alter drug availability and efficacy. |
|---|---|
| AbstractList | Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. However, the systematic mapping of the interactions between drugs and bacteria has only started recently.sup.1 and the main underlying mechanism proposed is the chemical transformation of drugs by microorganisms (biotransformation). Here we investigated the depletion of 15 structurally diverse drugs by 25 representative strains of gut bacteria. This revealed 70 bacteria-drug interactions, 29 of which had not to our knowledge been reported before. Over half of the new interactions can be ascribed to bioaccumulation; that is, bacteria storing the drug intracellularly without chemically modifying it, and in most cases without the growth of the bacteria being affected. As a case in point, we studied the molecular basis of bioaccumulation of the widely used antidepressant duloxetine by using click chemistry, thermal proteome profiling and metabolomics. We find that duloxetine binds to several metabolic enzymes and changes the metabolite secretion of the respective bacteria. When tested in a defined microbial community of accumulators and non-accumulators, duloxetine markedly altered the composition of the community through metabolic cross-feeding. We further validated our findings in an animal model, showing that bioaccumulating bacteria attenuate the behavioural response of Caenorhabditis elegans to duloxetine. Together, our results show that bioaccumulation by gut bacteria may be a common mechanism that alters drug availability and bacterial metabolism, with implications for microbiota composition, pharmacokinetics, side effects and drug responses, probably in an individual manner. Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. However, the systematic mapping of the interactions between drugs and bacteria has only started recently1 and the main underlying mechanism proposed is the chemical transformation of drugs by microorganisms (biotransformation). Here we investigated the depletion of 15 structurally diverse drugs by 25 representative strains of gut bacteria. This revealed 70 bacteria-drug interactions, 29 of which had not to our knowledge been reported before. Over half of the new interactions can be ascribed to bioaccumulation; that is, bacteria storing the drug intracellularly without chemically modifying it, and in most cases without the growth of the bacteria being affected. As a case in point, we studied the molecular basis of bioaccumulation of the widely used antidepressant duloxetine by using click chemistry, thermal proteome profiling and metabolomics. We find that duloxetine binds to several metabolic enzymes and changes the metabolite secretion of the respective bacteria. When tested in a defined microbial community of accumulators and non-accumulators, duloxetine markedly altered the composition of the community through metabolic cross-feeding. We further validated our findings in an animal model, showing that bioaccumulating bacteria attenuate the behavioural response of Caenorhabditis elegans to duloxetine. Together, our results show that bioaccumulation by gut bacteria may be a common mechanism that alters drug availability and bacterial metabolism, with implications for microbiota composition, pharmacokinetics, side effects and drug responses, probably in an individual manner.Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. However, the systematic mapping of the interactions between drugs and bacteria has only started recently1 and the main underlying mechanism proposed is the chemical transformation of drugs by microorganisms (biotransformation). Here we investigated the depletion of 15 structurally diverse drugs by 25 representative strains of gut bacteria. This revealed 70 bacteria-drug interactions, 29 of which had not to our knowledge been reported before. Over half of the new interactions can be ascribed to bioaccumulation; that is, bacteria storing the drug intracellularly without chemically modifying it, and in most cases without the growth of the bacteria being affected. As a case in point, we studied the molecular basis of bioaccumulation of the widely used antidepressant duloxetine by using click chemistry, thermal proteome profiling and metabolomics. We find that duloxetine binds to several metabolic enzymes and changes the metabolite secretion of the respective bacteria. When tested in a defined microbial community of accumulators and non-accumulators, duloxetine markedly altered the composition of the community through metabolic cross-feeding. We further validated our findings in an animal model, showing that bioaccumulating bacteria attenuate the behavioural response of Caenorhabditis elegans to duloxetine. Together, our results show that bioaccumulation by gut bacteria may be a common mechanism that alters drug availability and bacterial metabolism, with implications for microbiota composition, pharmacokinetics, side effects and drug responses, probably in an individual manner. Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. However, the systematic mapping of the interactions between drugs and bacteria has only started recently and the main underlying mechanism proposed is the chemical transformation of drugs by microorganisms (biotransformation). Here we investigated the depletion of 15 structurally diverse drugs by 25 representative strains of gut bacteria. This revealed 70 bacteria-drug interactions, 29 of which had not to our knowledge been reported before. Over half of the new interactions can be ascribed to bioaccumulation; that is, bacteria storing the drug intracellularly without chemically modifying it, and in most cases without the growth of the bacteria being affected. As a case in point, we studied the molecular basis of bioaccumulation of the widely used antidepressant duloxetine by using click chemistry, thermal proteome profiling and metabolomics. We find that duloxetine binds to several metabolic enzymes and changes the metabolite secretion of the respective bacteria. When tested in a defined microbial community of accumulators and non-accumulators, duloxetine markedly altered the composition of the community through metabolic cross-feeding. We further validated our findings in an animal model, showing that bioaccumulating bacteria attenuate the behavioural response of Caenorhabditis elegans to duloxetine. Together, our results show that bioaccumulation by gut bacteria may be a common mechanism that alters drug availability and bacterial metabolism, with implications for microbiota composition, pharmacokinetics, side effects and drug responses, probably in an individual manner. Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. However, the systematic mapping of the interactions between drugs and bacteria has only started recently.sup.1 and the main underlying mechanism proposed is the chemical transformation of drugs by microorganisms (biotransformation). Here we investigated the depletion of 15 structurally diverse drugs by 25 representative strains of gut bacteria. This revealed 70 bacteria-drug interactions, 29 of which had not to our knowledge been reported before. Over half of the new interactions can be ascribed to bioaccumulation; that is, bacteria storing the drug intracellularly without chemically modifying it, and in most cases without the growth of the bacteria being affected. As a case in point, we studied the molecular basis of bioaccumulation of the widely used antidepressant duloxetine by using click chemistry, thermal proteome profiling and metabolomics. We find that duloxetine binds to several metabolic enzymes and changes the metabolite secretion of the respective bacteria. When tested in a defined microbial community of accumulators and non-accumulators, duloxetine markedly altered the composition of the community through metabolic cross-feeding. We further validated our findings in an animal model, showing that bioaccumulating bacteria attenuate the behavioural response of Caenorhabditis elegans to duloxetine. Together, our results show that bioaccumulation by gut bacteria may be a common mechanism that alters drug availability and bacterial metabolism, with implications for microbiota composition, pharmacokinetics, side effects and drug responses, probably in an individual manner. An analysis of the interactions between 15 drugs and 25 gut bacterial strains shows that bioaccumulation of drugs within bacterial cells is another mechanism through which gut microorganisms can alter drug availability and efficacy. Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. Yet, the systematic mapping of the respective interactions has only started recently1 and the main underlying mechanism proposed is chemical transformation of drugs by microbes (biotransformation). Here, we investigated the depletion of 15 structurally diverse drugs by 25 representative gut bacterial strains. This revealed 70 bacteria-drug interactions, 29 of which had not been reported before. Over half of the new interactions can be ascribed to bioaccumulation, that is bacteria storing the drug intracellularly without chemically modifying it, and in most cases without their growth being affected. As a case in point, we studied the molecular basis of bioaccumulation of the widely used antidepressant duloxetine by using click-chemistry, thermal proteome profiling and metabolomics. We find that duloxetine binds to several metabolic enzymes and changes metabolite secretion of the respective bacteria. When tested in a defined microbial community of accumulators and non-accumulators, duloxetine markedly altered the community composition through metabolic cross-feeding. We further validated our findings in an animal model, showing that bioaccumulating bacteria attenuate the behavioral response of Caenorhabditis elegans to duloxetine. Taken together, bioaccumulation by gut bacteria may be a common mechanism that alters drug availability and bacterial metabolism, with implications for microbiota composition, pharmacokinetics, side effects and drug responses, likely in an individual manner. Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. However, the systematic mapping of the interactions between drugs and bacteria has only started recently1 and the main underlying mechanism proposed is the chemical transformation of drugs by microorganisms (biotransformation). Here we investigated the depletion of 15 structurally diverse drugs by 25 representative strains of gut bacteria. This revealed 70 bacteria-drug interactions, 29 of which had not to our knowledge been reported before. Over half of the new interactions can be ascribed to bioaccumulation; that is, bacteria storing the drug intracellularly without chemically modifying it, and in most cases without the growth of the bacteria being affected. As a case in point, we studied the molecular basis of bioaccumulation of the widely used antidepressant duloxetine by using click chemistry, thermal proteome profiling and metabolomics. We find that duloxetine binds to several metabolic enzymes and changes the metabolite secretion of the respective bacteria. When tested in a defined microbial community of accumulators and non-accumulators, duloxetine markedly altered the composition of the community through metabolic cross-feeding. We further validated our findings in an animal model, showing that bioaccumulating bacteria attenuate the behavioural response of Caenorhabditis elegans to duloxetine. Together, our results show that bioaccumulation by gut bacteria may be a common mechanism that alters drug availability and bacterial metabolism, with implications for microbiota composition, pharmacokinetics, side effects and drug responses, probably in an individual manner. Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. However, the systematic mapping of the interactions between drugs and bacteria has only started recently 1 and the main underlying mechanism proposed is the chemical transformation of drugs by microorganisms (biotransformation). Here we investigated the depletion of 15 structurally diverse drugs by 25 representative strains of gut bacteria. This revealed 70 bacteria–drug interactions, 29 of which had not to our knowledge been reported before. Over half of the new interactions can be ascribed to bioaccumulation; that is, bacteria storing the drug intracellularly without chemically modifying it, and in most cases without the growth of the bacteria being affected. As a case in point, we studied the molecular basis of bioaccumulation of the widely used antidepressant duloxetine by using click chemistry, thermal proteome profiling and metabolomics. We find that duloxetine binds to several metabolic enzymes and changes the metabolite secretion of the respective bacteria. When tested in a defined microbial community of accumulators and non-accumulators, duloxetine markedly altered the composition of the community through metabolic cross-feeding. We further validated our findings in an animal model, showing that bioaccumulating bacteria attenuate the behavioural response of Caenorhabditis elegans to duloxetine. Together, our results show that bioaccumulation by gut bacteria may be a common mechanism that alters drug availability and bacterial metabolism, with implications for microbiota composition, pharmacokinetics, side effects and drug responses, probably in an individual manner. An analysis of the interactions between 15 drugs and 25 gut bacterial strains shows that bioaccumulation of drugs within bacterial cells is another mechanism through which gut microorganisms can alter drug availability and efficacy. |
| Audience | Academic |
| Author | Phapale, Prasad Kafkia, Eleni Hennig, Janosch Periwal, Vinita Cabreiro, Filipe Zimmermann, Michael Bork, Peer Maier, Lisa Andrejev, Sergej Simon, Bernd Zirngibl, Katharina Kim, Yongkyu Nesme, Leo Blasche, Sonja Savitski, Mikhail M. Klünemann, Martina Hövelmann, Felix Kumar, Manjeet Bock, Thomas Typas, Athanasios Mackmull, Marie-Therese Patil, Kiran R. Banzhaf, Manuel Vappiani, Johanna Mateus, Andre Tramontano, Melanie Konstantinidis, Dimitrios Mastrorilli, Eleonora Scott, Timothy A. Beck, Martin Sévin, Daniel C. Brochado, Ana Rita Schultz, Carsten Devendran, Saravanan |
| AuthorAffiliation | 3 Cellzome, GlaxoSmithKline R&D, Heidelberg, Germany 12 Institute of Clinical Sciences, Imperial College London, UK 14 Max Delbrück Centre for Molecular Medicine, Berlin, Germany 17 Medical Research Council Toxicology Unit, Cambridge, United Kingdom 1 European Molecular Biology Laboratory, Heidelberg, Germany 16 Department of Bioinformatics, Biocenter, University of Würzburg, Würzburg, Germany 2 Institute of Structural and Molecular Biology, University College London, UK 15 Yonsei Frontier Lab (YFL), Yonsei University, Seoul 03722, South Korea |
| AuthorAffiliation_xml | – name: 17 Medical Research Council Toxicology Unit, Cambridge, United Kingdom – name: 3 Cellzome, GlaxoSmithKline R&D, Heidelberg, Germany – name: 1 European Molecular Biology Laboratory, Heidelberg, Germany – name: 2 Institute of Structural and Molecular Biology, University College London, UK – name: 15 Yonsei Frontier Lab (YFL), Yonsei University, Seoul 03722, South Korea – name: 12 Institute of Clinical Sciences, Imperial College London, UK – name: 14 Max Delbrück Centre for Molecular Medicine, Berlin, Germany – name: 16 Department of Bioinformatics, Biocenter, University of Würzburg, Würzburg, Germany |
| Author_xml | – sequence: 1 givenname: Martina orcidid: 0000-0002-1602-5371 surname: Klünemann fullname: Klünemann, Martina organization: European Molecular Biology Laboratory, Evonik Operations GmbH – sequence: 2 givenname: Sergej orcidid: 0000-0002-7875-0261 surname: Andrejev fullname: Andrejev, Sergej organization: European Molecular Biology Laboratory, German Cancer Research Center – sequence: 3 givenname: Sonja surname: Blasche fullname: Blasche, Sonja organization: European Molecular Biology Laboratory, Medical Research Council Toxicology Unit – sequence: 4 givenname: Andre orcidid: 0000-0001-6870-0677 surname: Mateus fullname: Mateus, Andre organization: European Molecular Biology Laboratory – sequence: 5 givenname: Prasad orcidid: 0000-0002-9487-597X surname: Phapale fullname: Phapale, Prasad organization: European Molecular Biology Laboratory – sequence: 6 givenname: Saravanan surname: Devendran fullname: Devendran, Saravanan organization: European Molecular Biology Laboratory – sequence: 7 givenname: Johanna surname: Vappiani fullname: Vappiani, Johanna organization: Cellzome, GlaxoSmithKline R&D – sequence: 8 givenname: Bernd surname: Simon fullname: Simon, Bernd organization: European Molecular Biology Laboratory – sequence: 9 givenname: Timothy A. surname: Scott fullname: Scott, Timothy A. organization: Institute of Structural and Molecular Biology, University College London – sequence: 10 givenname: Eleni orcidid: 0000-0001-9550-4487 surname: Kafkia fullname: Kafkia, Eleni organization: Medical Research Council Toxicology Unit – sequence: 11 givenname: Dimitrios surname: Konstantinidis fullname: Konstantinidis, Dimitrios organization: European Molecular Biology Laboratory – sequence: 12 givenname: Katharina surname: Zirngibl fullname: Zirngibl, Katharina organization: European Molecular Biology Laboratory, Medical Research Council Toxicology Unit – sequence: 13 givenname: Eleonora orcidid: 0000-0003-2127-4150 surname: Mastrorilli fullname: Mastrorilli, Eleonora organization: European Molecular Biology Laboratory – sequence: 14 givenname: Manuel surname: Banzhaf fullname: Banzhaf, Manuel organization: European Molecular Biology Laboratory, School of Biosciences, University of Birmingham – sequence: 15 givenname: Marie-Therese orcidid: 0000-0003-2928-1144 surname: Mackmull fullname: Mackmull, Marie-Therese organization: European Molecular Biology Laboratory, ETH Zürich – sequence: 16 givenname: Felix surname: Hövelmann fullname: Hövelmann, Felix organization: European Molecular Biology Laboratory – sequence: 17 givenname: Leo surname: Nesme fullname: Nesme, Leo organization: European Molecular Biology Laboratory, Molecular Health GmbH – sequence: 18 givenname: Ana Rita surname: Brochado fullname: Brochado, Ana Rita organization: European Molecular Biology Laboratory, University of Würzburg – sequence: 19 givenname: Lisa orcidid: 0000-0002-6473-4762 surname: Maier fullname: Maier, Lisa organization: European Molecular Biology Laboratory, University of Tübingen – sequence: 20 givenname: Thomas orcidid: 0000-0002-9314-5318 surname: Bock fullname: Bock, Thomas organization: European Molecular Biology Laboratory, Biozentrum, University of Basel – sequence: 21 givenname: Vinita surname: Periwal fullname: Periwal, Vinita organization: European Molecular Biology Laboratory, Medical Research Council Toxicology Unit – sequence: 22 givenname: Manjeet surname: Kumar fullname: Kumar, Manjeet organization: European Molecular Biology Laboratory – sequence: 23 givenname: Yongkyu orcidid: 0000-0002-3336-6741 surname: Kim fullname: Kim, Yongkyu organization: European Molecular Biology Laboratory – sequence: 24 givenname: Melanie orcidid: 0000-0001-6407-527X surname: Tramontano fullname: Tramontano, Melanie organization: European Molecular Biology Laboratory, German Cancer Research Center – sequence: 25 givenname: Carsten surname: Schultz fullname: Schultz, Carsten organization: European Molecular Biology Laboratory, Chemical Physiology and Biochemistry Department, Oregon Health & Science University, Portland – sequence: 26 givenname: Martin orcidid: 0000-0002-7397-1321 surname: Beck fullname: Beck, Martin organization: European Molecular Biology Laboratory, Max Planck Institute of Biophysics – sequence: 27 givenname: Janosch orcidid: 0000-0001-5214-7002 surname: Hennig fullname: Hennig, Janosch organization: European Molecular Biology Laboratory, Biophysical Chemistry Department, University of Bayreuth – sequence: 28 givenname: Michael orcidid: 0000-0002-5797-3589 surname: Zimmermann fullname: Zimmermann, Michael organization: European Molecular Biology Laboratory – sequence: 29 givenname: Daniel C. surname: Sévin fullname: Sévin, Daniel C. organization: Cellzome, GlaxoSmithKline R&D – sequence: 30 givenname: Filipe orcidid: 0000-0002-3696-4843 surname: Cabreiro fullname: Cabreiro, Filipe organization: Institute of Structural and Molecular Biology, University College London, Institute of Clinical Sciences, Imperial College London, CECAD, University of Cologne – sequence: 31 givenname: Mikhail M. orcidid: 0000-0003-2011-9247 surname: Savitski fullname: Savitski, Mikhail M. organization: European Molecular Biology Laboratory – sequence: 32 givenname: Peer orcidid: 0000-0002-2627-833X surname: Bork fullname: Bork, Peer email: bork@embl.de organization: European Molecular Biology Laboratory, Max Delbrück Centre for Molecular Medicine, Yonsei Frontier Lab (YFL), Yonsei University, Department of Bioinformatics, Biocenter, University of Würzburg – sequence: 33 givenname: Athanasios orcidid: 0000-0002-0797-9018 surname: Typas fullname: Typas, Athanasios email: typas@embl.de organization: European Molecular Biology Laboratory – sequence: 34 givenname: Kiran R. orcidid: 0000-0002-6166-8640 surname: Patil fullname: Patil, Kiran R. email: kp533@cam.ac.uk organization: European Molecular Biology Laboratory, Medical Research Council Toxicology Unit |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34497420$$D View this record in MEDLINE/PubMed |
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| Snippet | Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. However, the systematic mapping of the interactions between drugs and... Bacteria in the gut can modulate the availability and efficacy of therapeutic drugs. Yet, the systematic mapping of the respective interactions has only... |
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| Title | Bioaccumulation of therapeutic drugs by human gut bacteria |
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