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A Master Regulator of Bacteroides thetaiotaomicron Gut Colonization Controls Carbohydrate Utilization and an Alternative Protein Synthesis Factor

Microbial colonization of the mammalian gut is largely ascribed to the ability to utilize nutrients available in that environment. To understand how beneficial microbes establish a relationship with their hosts, it is crucial to determine what other abilities promote gut colonization. We now report...

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Autores principales: Townsend, Guy E., Han, Weiwei, Schwalm, Nathan D., Hong, Xinyu, Bencivenga-Barry, Natasha A., Goodman, Andrew L., Groisman, Eduardo A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6989115/
https://www.ncbi.nlm.nih.gov/pubmed/31992627
http://dx.doi.org/10.1128/mBio.03221-19
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author Townsend, Guy E.
Han, Weiwei
Schwalm, Nathan D.
Hong, Xinyu
Bencivenga-Barry, Natasha A.
Goodman, Andrew L.
Groisman, Eduardo A.
author_facet Townsend, Guy E.
Han, Weiwei
Schwalm, Nathan D.
Hong, Xinyu
Bencivenga-Barry, Natasha A.
Goodman, Andrew L.
Groisman, Eduardo A.
author_sort Townsend, Guy E.
collection PubMed
description Microbial colonization of the mammalian gut is largely ascribed to the ability to utilize nutrients available in that environment. To understand how beneficial microbes establish a relationship with their hosts, it is crucial to determine what other abilities promote gut colonization. We now report that colonization of the murine gut by the beneficial microbe Bacteroides thetaiotaomicron requires activation of a putative translation factor by the major transcriptional regulator of gut colonization and carbohydrate utilization. To ascertain how this regulator—called BT4338—promotes gut colonization, we identified BT4338-regulated genes and BT4338-bound DNA sequences. Unexpectedly, the gene whose expression was most reduced upon BT4338 inactivation was fusA2, specifying a putative translation factor. We determined that fusA2 activation by BT4338 is conserved in another Bacteroides species and essential for gut colonization in B. thetaiotaomicron because a mutant lacking the BT4338 binding site in the fusA2 promoter exhibited a colonization defect similar to that of a mutant lacking the fusA2 gene. Furthermore, we demonstrated that BT4338 promotes gut colonization independently of its role in carbohydrate utilization because the fusA2 gene was dispensable for utilization of carbohydrates that depend on BT4338. Our findings suggest that microbial gut colonization requires the use of alternative protein synthesis factors.
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spelling pubmed-69891152020-02-04 A Master Regulator of Bacteroides thetaiotaomicron Gut Colonization Controls Carbohydrate Utilization and an Alternative Protein Synthesis Factor Townsend, Guy E. Han, Weiwei Schwalm, Nathan D. Hong, Xinyu Bencivenga-Barry, Natasha A. Goodman, Andrew L. Groisman, Eduardo A. mBio Research Article Microbial colonization of the mammalian gut is largely ascribed to the ability to utilize nutrients available in that environment. To understand how beneficial microbes establish a relationship with their hosts, it is crucial to determine what other abilities promote gut colonization. We now report that colonization of the murine gut by the beneficial microbe Bacteroides thetaiotaomicron requires activation of a putative translation factor by the major transcriptional regulator of gut colonization and carbohydrate utilization. To ascertain how this regulator—called BT4338—promotes gut colonization, we identified BT4338-regulated genes and BT4338-bound DNA sequences. Unexpectedly, the gene whose expression was most reduced upon BT4338 inactivation was fusA2, specifying a putative translation factor. We determined that fusA2 activation by BT4338 is conserved in another Bacteroides species and essential for gut colonization in B. thetaiotaomicron because a mutant lacking the BT4338 binding site in the fusA2 promoter exhibited a colonization defect similar to that of a mutant lacking the fusA2 gene. Furthermore, we demonstrated that BT4338 promotes gut colonization independently of its role in carbohydrate utilization because the fusA2 gene was dispensable for utilization of carbohydrates that depend on BT4338. Our findings suggest that microbial gut colonization requires the use of alternative protein synthesis factors. American Society for Microbiology 2020-01-28 /pmc/articles/PMC6989115/ /pubmed/31992627 http://dx.doi.org/10.1128/mBio.03221-19 Text en Copyright © 2020 Townsend et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Townsend, Guy E.
Han, Weiwei
Schwalm, Nathan D.
Hong, Xinyu
Bencivenga-Barry, Natasha A.
Goodman, Andrew L.
Groisman, Eduardo A.
A Master Regulator of Bacteroides thetaiotaomicron Gut Colonization Controls Carbohydrate Utilization and an Alternative Protein Synthesis Factor
title A Master Regulator of Bacteroides thetaiotaomicron Gut Colonization Controls Carbohydrate Utilization and an Alternative Protein Synthesis Factor
title_full A Master Regulator of Bacteroides thetaiotaomicron Gut Colonization Controls Carbohydrate Utilization and an Alternative Protein Synthesis Factor
title_fullStr A Master Regulator of Bacteroides thetaiotaomicron Gut Colonization Controls Carbohydrate Utilization and an Alternative Protein Synthesis Factor
title_full_unstemmed A Master Regulator of Bacteroides thetaiotaomicron Gut Colonization Controls Carbohydrate Utilization and an Alternative Protein Synthesis Factor
title_short A Master Regulator of Bacteroides thetaiotaomicron Gut Colonization Controls Carbohydrate Utilization and an Alternative Protein Synthesis Factor
title_sort master regulator of bacteroides thetaiotaomicron gut colonization controls carbohydrate utilization and an alternative protein synthesis factor
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6989115/
https://www.ncbi.nlm.nih.gov/pubmed/31992627
http://dx.doi.org/10.1128/mBio.03221-19
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