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Bacterial Microcompartment-Dependent 1,2-Propanediol Utilization of Propionibacterium freudenreichii

Bacterial microcompartments (BMCs) are proteinaceous prokaryotic organelles that enable the utilization of substrates such as 1,2-propanediol and ethanolamine. BMCs are mostly linked to the survival of particular pathogenic bacteria by providing a growth advantage through utilization of 1,2-propaned...

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Autores principales: Dank, Alexander, Zeng, Zhe, Boeren, Sjef, Notebaart, Richard A., Smid, Eddy J., Abee, Tjakko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8149966/
https://www.ncbi.nlm.nih.gov/pubmed/34054787
http://dx.doi.org/10.3389/fmicb.2021.679827
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author Dank, Alexander
Zeng, Zhe
Boeren, Sjef
Notebaart, Richard A.
Smid, Eddy J.
Abee, Tjakko
author_facet Dank, Alexander
Zeng, Zhe
Boeren, Sjef
Notebaart, Richard A.
Smid, Eddy J.
Abee, Tjakko
author_sort Dank, Alexander
collection PubMed
description Bacterial microcompartments (BMCs) are proteinaceous prokaryotic organelles that enable the utilization of substrates such as 1,2-propanediol and ethanolamine. BMCs are mostly linked to the survival of particular pathogenic bacteria by providing a growth advantage through utilization of 1,2-propanediol and ethanolamine which are abundantly present in the human gut. Although a 1,2-propanediol utilization cluster was found in the probiotic bacterium Propionibacterium freudenreichii, BMC-mediated metabolism of 1,2-propanediol has not been demonstrated experimentally in P. freudenreichii. In this study we show that P. freudenreichii DSM 20271 metabolizes 1,2-propanediol in anaerobic conditions to propionate and 1-propanol. Furthermore, 1,2-propanediol induced the formation of BMCs, which were visualized by transmission electron microscopy and resembled BMCs found in other bacteria. Proteomic analysis of 1,2-propanediol grown cells compared to L-lactate grown cells showed significant upregulation of proteins involved in propanediol-utilization (pdu-cluster), DNA repair mechanisms and BMC shell proteins while proteins involved in oxidative phosphorylation were down-regulated. 1,2-Propanediol utilizing cells actively produced vitamin B(12) (cobalamin) in similar amounts as cells growing on L-lactate. The ability to metabolize 1,2-propanediol may have implications for human gut colonization and modulation, and can potentially aid in delivering propionate and vitamin B(12) in situ.
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spelling pubmed-81499662021-05-27 Bacterial Microcompartment-Dependent 1,2-Propanediol Utilization of Propionibacterium freudenreichii Dank, Alexander Zeng, Zhe Boeren, Sjef Notebaart, Richard A. Smid, Eddy J. Abee, Tjakko Front Microbiol Microbiology Bacterial microcompartments (BMCs) are proteinaceous prokaryotic organelles that enable the utilization of substrates such as 1,2-propanediol and ethanolamine. BMCs are mostly linked to the survival of particular pathogenic bacteria by providing a growth advantage through utilization of 1,2-propanediol and ethanolamine which are abundantly present in the human gut. Although a 1,2-propanediol utilization cluster was found in the probiotic bacterium Propionibacterium freudenreichii, BMC-mediated metabolism of 1,2-propanediol has not been demonstrated experimentally in P. freudenreichii. In this study we show that P. freudenreichii DSM 20271 metabolizes 1,2-propanediol in anaerobic conditions to propionate and 1-propanol. Furthermore, 1,2-propanediol induced the formation of BMCs, which were visualized by transmission electron microscopy and resembled BMCs found in other bacteria. Proteomic analysis of 1,2-propanediol grown cells compared to L-lactate grown cells showed significant upregulation of proteins involved in propanediol-utilization (pdu-cluster), DNA repair mechanisms and BMC shell proteins while proteins involved in oxidative phosphorylation were down-regulated. 1,2-Propanediol utilizing cells actively produced vitamin B(12) (cobalamin) in similar amounts as cells growing on L-lactate. The ability to metabolize 1,2-propanediol may have implications for human gut colonization and modulation, and can potentially aid in delivering propionate and vitamin B(12) in situ. Frontiers Media S.A. 2021-05-12 /pmc/articles/PMC8149966/ /pubmed/34054787 http://dx.doi.org/10.3389/fmicb.2021.679827 Text en Copyright © 2021 Dank, Zeng, Boeren, Notebaart, Smid and Abee. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Dank, Alexander
Zeng, Zhe
Boeren, Sjef
Notebaart, Richard A.
Smid, Eddy J.
Abee, Tjakko
Bacterial Microcompartment-Dependent 1,2-Propanediol Utilization of Propionibacterium freudenreichii
title Bacterial Microcompartment-Dependent 1,2-Propanediol Utilization of Propionibacterium freudenreichii
title_full Bacterial Microcompartment-Dependent 1,2-Propanediol Utilization of Propionibacterium freudenreichii
title_fullStr Bacterial Microcompartment-Dependent 1,2-Propanediol Utilization of Propionibacterium freudenreichii
title_full_unstemmed Bacterial Microcompartment-Dependent 1,2-Propanediol Utilization of Propionibacterium freudenreichii
title_short Bacterial Microcompartment-Dependent 1,2-Propanediol Utilization of Propionibacterium freudenreichii
title_sort bacterial microcompartment-dependent 1,2-propanediol utilization of propionibacterium freudenreichii
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8149966/
https://www.ncbi.nlm.nih.gov/pubmed/34054787
http://dx.doi.org/10.3389/fmicb.2021.679827
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