The Proteome of Extracellular Vesicles Produced by the Human Gut Bacteria Bacteroides thetaiotaomicron In Vivo Is Influenced by Environmental and Host-Derived Factors

Stentz, Régis, Jones, Emily, Juodeikis, Rokas, Wegmann, Udo, Guirro, Maria, Goldson, Andrew J., Brion, Arlaine, Booth, Catherine, Sudhakar, Padhmanand, Brown, Ian R., Korcsmáros, Tamás and Carding, Simon R. (2022) The Proteome of Extracellular Vesicles Produced by the Human Gut Bacteria Bacteroides thetaiotaomicron In Vivo Is Influenced by Environmental and Host-Derived Factors. Applied and Environmental Microbiology, 88 (16). ISSN 0099-2240

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Abstract

Bacterial extracellular vesicles (BEVs) released from both Gram-negative and Gram-positive bacteria provide an effective means of communication and trafficking of cell signaling molecules. In the gastrointestinal tract (GIT) BEVs produced by members of the intestinal microbiota can impact host health by mediating microbe-host cell interactions. A major unresolved question, however, is what factors influence the composition of BEV proteins and whether the host influences protein packaging into BEVs and secretion into the GIT. To address this, we have analyzed the proteome of BEVs produced by the major human gut symbiont Bacteroides thetaiotaomicron both in vitro and in vivo in the murine GIT in order to identify proteins specifically enriched in BEVs produced in vivo. We identified 113 proteins enriched in BEVs produced in vivo, the majority (62/113) of which accumulated in BEVs in the absence of any changes in their expression by the parental cells. Among these selectively enriched proteins, we identified dipeptidyl peptidases and an asparaginase and confirmed their increased activity in BEVs produced in vivo. We also showed that intact BEVs are capable of degrading bile acids via a bile salt hydrolase. Collectively these findings provide additional evidence for the dynamic interplay of host-microbe interactions in the GIT and the existence of an active mechanism to drive and enrich a selected group of proteins for secretion into BEVs in the GIT.

Item Type: Article
Additional Information: Funding Information: This work was supported in part by the UK Biotechnology and Biological Sciences Research Council (BBSRC) under grant numbers BB/J004529/1, BB/R012490/1, and BBS/E/F000PR10355 (S.R.C.). The work of T.K. was supported by the Earlham Institute (Norwich, UK) in partnership with the Quadram Institute (Norwich, UK) and strategically supported by a UKRI BBSRC UK grant (BB/CSP17270/1). T.K. and P.S. were also supported by a BBSRC ISP grant for Gut Microbes and Health BB/R012490/1 and its constituent projects, BBS/E/F/000PR10353 and BBS/E/F/000PR10355. Publisher Copyright: 2022 Stentz et al.
Uncontrolled Keywords: bacterial extracellular vesicles,bacteroides thetaiotaomicron,intestine,microbiota,proteome,biotechnology,food science,ecology,applied microbiology and biotechnology,sdg 3 - good health and well-being ,/dk/atira/pure/subjectarea/asjc/1300/1305
Faculty \ School: Faculty of Science > School of Chemistry
Faculty of Science > School of Biological Sciences
Faculty of Medicine and Health Sciences > Norwich Medical School
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Depositing User: LivePure Connector
Date Deposited: 07 Nov 2022 09:30
Last Modified: 07 Nov 2022 09:30
URI: https://ueaeprints.uea.ac.uk/id/eprint/89671
DOI: 10.1128/aem.00533-22

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