Nutrient smuggling: Commensal gut bacteria‐derived extracellular vesicles scavenge vitamin B12 and related cobamides for microbe and host acquisition

Abstract The processes by which bacteria proactively scavenge essential nutrients in crowded environments such as the gastrointestinal tract are not fully understood. In this context, we observed that bacterial extracellular vesicles (BEVs) produced by the human commensal gut microbe Bacteroides the...

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Main Authors: Rokas Juodeikis, Emily Jones, Evelyne Deery, David M. Beal, Régis Stentz, Bernhard Kräutler, Simon R. Carding, Martin J. Warren
Format: Article
Language:English
Published: Wiley 2022-10-01
Series:Journal of Extracellular Biology
Subjects:
Online Access:https://doi.org/10.1002/jex2.61
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author Rokas Juodeikis
Emily Jones
Evelyne Deery
David M. Beal
Régis Stentz
Bernhard Kräutler
Simon R. Carding
Martin J. Warren
author_facet Rokas Juodeikis
Emily Jones
Evelyne Deery
David M. Beal
Régis Stentz
Bernhard Kräutler
Simon R. Carding
Martin J. Warren
author_sort Rokas Juodeikis
collection DOAJ
description Abstract The processes by which bacteria proactively scavenge essential nutrients in crowded environments such as the gastrointestinal tract are not fully understood. In this context, we observed that bacterial extracellular vesicles (BEVs) produced by the human commensal gut microbe Bacteroides thetaiotaomicron contain multiple high‐affinity vitamin B12 binding proteins suggesting that the vesicles play a role in micronutrient scavenging. Vitamin B12 belongs to the cobamide family of cofactors that regulate microbial communities through their limited bioavailability. We show that B. thetaiotaomicron derived BEVs bind a variety of cobamides and not only deliver them back to the parental bacterium but also sequester the micronutrient from competing bacteria. Additionally, Caco‐2 cells, representing a model intestinal epithelial barrier, acquire cobamide‐bound vesicles and traffic them to lysosomes, thereby mimicking the physiological cobalamin‐specific intrinsic factor‐mediated uptake process. Our findings identify a novel cobamide binding activity associated with BEVs with far‐reaching implications for microbiota and host health.
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spelling doaj.art-f962e70a581543c99ec025772fd014f82023-08-01T18:56:01ZengWileyJournal of Extracellular Biology2768-28112022-10-01110n/an/a10.1002/jex2.61Nutrient smuggling: Commensal gut bacteria‐derived extracellular vesicles scavenge vitamin B12 and related cobamides for microbe and host acquisitionRokas Juodeikis0Emily Jones1Evelyne Deery2David M. Beal3Régis Stentz4Bernhard Kräutler5Simon R. Carding6Martin J. Warren7Quadram Institute Bioscience Norwich UKQuadram Institute Bioscience Norwich UKSchool of Biosciences University of Kent Canterbury Kent UKSchool of Biosciences University of Kent Canterbury Kent UKQuadram Institute Bioscience Norwich UKInstitute of Organic Chemistry and Centre for Molecular Biosciences University of Innsbruck Innsbruck AustriaQuadram Institute Bioscience Norwich UKQuadram Institute Bioscience Norwich UKAbstract The processes by which bacteria proactively scavenge essential nutrients in crowded environments such as the gastrointestinal tract are not fully understood. In this context, we observed that bacterial extracellular vesicles (BEVs) produced by the human commensal gut microbe Bacteroides thetaiotaomicron contain multiple high‐affinity vitamin B12 binding proteins suggesting that the vesicles play a role in micronutrient scavenging. Vitamin B12 belongs to the cobamide family of cofactors that regulate microbial communities through their limited bioavailability. We show that B. thetaiotaomicron derived BEVs bind a variety of cobamides and not only deliver them back to the parental bacterium but also sequester the micronutrient from competing bacteria. Additionally, Caco‐2 cells, representing a model intestinal epithelial barrier, acquire cobamide‐bound vesicles and traffic them to lysosomes, thereby mimicking the physiological cobalamin‐specific intrinsic factor‐mediated uptake process. Our findings identify a novel cobamide binding activity associated with BEVs with far‐reaching implications for microbiota and host health.https://doi.org/10.1002/jex2.61bacterial extracellular vesiclesbacteroidescobamidesmicrobe–host interactionnutrient uptakevitamin B12
spellingShingle Rokas Juodeikis
Emily Jones
Evelyne Deery
David M. Beal
Régis Stentz
Bernhard Kräutler
Simon R. Carding
Martin J. Warren
Nutrient smuggling: Commensal gut bacteria‐derived extracellular vesicles scavenge vitamin B12 and related cobamides for microbe and host acquisition
Journal of Extracellular Biology
bacterial extracellular vesicles
bacteroides
cobamides
microbe–host interaction
nutrient uptake
vitamin B12
title Nutrient smuggling: Commensal gut bacteria‐derived extracellular vesicles scavenge vitamin B12 and related cobamides for microbe and host acquisition
title_full Nutrient smuggling: Commensal gut bacteria‐derived extracellular vesicles scavenge vitamin B12 and related cobamides for microbe and host acquisition
title_fullStr Nutrient smuggling: Commensal gut bacteria‐derived extracellular vesicles scavenge vitamin B12 and related cobamides for microbe and host acquisition
title_full_unstemmed Nutrient smuggling: Commensal gut bacteria‐derived extracellular vesicles scavenge vitamin B12 and related cobamides for microbe and host acquisition
title_short Nutrient smuggling: Commensal gut bacteria‐derived extracellular vesicles scavenge vitamin B12 and related cobamides for microbe and host acquisition
title_sort nutrient smuggling commensal gut bacteria derived extracellular vesicles scavenge vitamin b12 and related cobamides for microbe and host acquisition
topic bacterial extracellular vesicles
bacteroides
cobamides
microbe–host interaction
nutrient uptake
vitamin B12
url https://doi.org/10.1002/jex2.61
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