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BtuB TonB-dependent transporters and BtuG surface lipoproteins form stable complexes for vitamin B(12) uptake in gut Bacteroides

Vitamin B(12) (cobalamin) is required for most human gut microbes, many of which are dependent on scavenging to obtain this vitamin. Since bacterial densities in the gut are extremely high, competition for this keystone micronutrient is severe. Contrasting with Enterobacteria, members of the dominan...

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Autores principales: Abellon-Ruiz, Javier, Jana, Kalyanashis, Silale, Augustinas, Frey, Andrew M., Baslé, Arnaud, Trost, Matthias, Kleinekathöfer, Ulrich, van den Berg, Bert
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10404256/
https://www.ncbi.nlm.nih.gov/pubmed/37543597
http://dx.doi.org/10.1038/s41467-023-40427-2
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author Abellon-Ruiz, Javier
Jana, Kalyanashis
Silale, Augustinas
Frey, Andrew M.
Baslé, Arnaud
Trost, Matthias
Kleinekathöfer, Ulrich
van den Berg, Bert
author_facet Abellon-Ruiz, Javier
Jana, Kalyanashis
Silale, Augustinas
Frey, Andrew M.
Baslé, Arnaud
Trost, Matthias
Kleinekathöfer, Ulrich
van den Berg, Bert
author_sort Abellon-Ruiz, Javier
collection PubMed
description Vitamin B(12) (cobalamin) is required for most human gut microbes, many of which are dependent on scavenging to obtain this vitamin. Since bacterial densities in the gut are extremely high, competition for this keystone micronutrient is severe. Contrasting with Enterobacteria, members of the dominant genus Bacteroides often encode several BtuB vitamin B(12) outer membrane transporters together with a conserved array of surface-exposed B(12)-binding lipoproteins. Here we show that the BtuB transporters from Bacteroides thetaiotaomicron form stable, pedal bin-like complexes with surface-exposed BtuG lipoprotein lids, which bind B(12) with high affinities. Closing of the BtuG lid following B(12) capture causes destabilisation of the bound B(12) by a conserved BtuB extracellular loop, causing translocation of the vitamin to BtuB and subsequent transport. We propose that TonB-dependent, lipoprotein-assisted small molecule uptake is a general feature of Bacteroides spp. that is important for the success of this genus in colonising the human gut.
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spelling pubmed-104042562023-08-07 BtuB TonB-dependent transporters and BtuG surface lipoproteins form stable complexes for vitamin B(12) uptake in gut Bacteroides Abellon-Ruiz, Javier Jana, Kalyanashis Silale, Augustinas Frey, Andrew M. Baslé, Arnaud Trost, Matthias Kleinekathöfer, Ulrich van den Berg, Bert Nat Commun Article Vitamin B(12) (cobalamin) is required for most human gut microbes, many of which are dependent on scavenging to obtain this vitamin. Since bacterial densities in the gut are extremely high, competition for this keystone micronutrient is severe. Contrasting with Enterobacteria, members of the dominant genus Bacteroides often encode several BtuB vitamin B(12) outer membrane transporters together with a conserved array of surface-exposed B(12)-binding lipoproteins. Here we show that the BtuB transporters from Bacteroides thetaiotaomicron form stable, pedal bin-like complexes with surface-exposed BtuG lipoprotein lids, which bind B(12) with high affinities. Closing of the BtuG lid following B(12) capture causes destabilisation of the bound B(12) by a conserved BtuB extracellular loop, causing translocation of the vitamin to BtuB and subsequent transport. We propose that TonB-dependent, lipoprotein-assisted small molecule uptake is a general feature of Bacteroides spp. that is important for the success of this genus in colonising the human gut. Nature Publishing Group UK 2023-08-05 /pmc/articles/PMC10404256/ /pubmed/37543597 http://dx.doi.org/10.1038/s41467-023-40427-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Abellon-Ruiz, Javier
Jana, Kalyanashis
Silale, Augustinas
Frey, Andrew M.
Baslé, Arnaud
Trost, Matthias
Kleinekathöfer, Ulrich
van den Berg, Bert
BtuB TonB-dependent transporters and BtuG surface lipoproteins form stable complexes for vitamin B(12) uptake in gut Bacteroides
title BtuB TonB-dependent transporters and BtuG surface lipoproteins form stable complexes for vitamin B(12) uptake in gut Bacteroides
title_full BtuB TonB-dependent transporters and BtuG surface lipoproteins form stable complexes for vitamin B(12) uptake in gut Bacteroides
title_fullStr BtuB TonB-dependent transporters and BtuG surface lipoproteins form stable complexes for vitamin B(12) uptake in gut Bacteroides
title_full_unstemmed BtuB TonB-dependent transporters and BtuG surface lipoproteins form stable complexes for vitamin B(12) uptake in gut Bacteroides
title_short BtuB TonB-dependent transporters and BtuG surface lipoproteins form stable complexes for vitamin B(12) uptake in gut Bacteroides
title_sort btub tonb-dependent transporters and btug surface lipoproteins form stable complexes for vitamin b(12) uptake in gut bacteroides
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10404256/
https://www.ncbi.nlm.nih.gov/pubmed/37543597
http://dx.doi.org/10.1038/s41467-023-40427-2
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