Thiamine Acquisition Strategies Impact Metabolism and Competition in the Gut Microbe <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>

ABSTRACT Thiamine (vitamin B1) is an essential cofactor for all organisms. Humans primarily acquire thiamine through their diet, and thiamine deficiencies have adverse neurological effects. However, the role gut microbes play in modulating thiamine availability is poorly understood, and little is kn...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Zachary A. Costliow, Patrick H. Degnan
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	competition microbiome pnuT thiamine pyrophosphate (TPP) vitamin B1 Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8f0dc9063eaa45e189acf3a05182d9e9
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:8f0dc9063eaa45e189acf3a05182d9e9
record_format	dspace
spelling	oai:doaj.org-article:8f0dc9063eaa45e189acf3a05182d9e92021-12-02T19:45:29ZThiamine Acquisition Strategies Impact Metabolism and Competition in the Gut Microbe <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>10.1128/mSystems.00116-172379-5077https://doaj.org/article/8f0dc9063eaa45e189acf3a05182d9e92017-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00116-17https://doaj.org/toc/2379-5077ABSTRACT Thiamine (vitamin B1) is an essential cofactor for all organisms. Humans primarily acquire thiamine through their diet, and thiamine deficiencies have adverse neurological effects. However, the role gut microbes play in modulating thiamine availability is poorly understood, and little is known about how thiamine impacts the stability of microbial gut communities. To investigate thiamine’s role in the gut, we utilized the model gut microbe Bacteroides thetaiotaomicron. Transcriptome sequencing (RNA-seq) revealed a global downregulation of thiamine and amino acid biosynthesis, glycolysis, and purine metabolism when thiamine was present. Using genetic mutants with thiamine biosynthesis and transport locus mutations, we determined both systems were critical for growth in thiamine-deficient medium. The defect in the double transport mutant suggests an uncharacterized feedback mechanism between thiamine transport and biosynthesis in B. thetaiotaomicron. Mutant phenotypes were recapitulated during pairwise competitions, reinforcing the importance of encoding versatile thiamine acquisition mechanisms when thiamine concentrations are variable. In addition, liquid chromatography-mass spectrometry (LC-MS) analyses corroborate that exogenous thiamine levels affect the internal thiamine pool of B. thetaiotaomicron. Furthermore, we computationally examined the ability of other gut microbes to acquire thiamine and identified lineage-specific differences in thiamine acquisition strategies. Among the Bacteroidetes, the capacities for both thiamine transport and biosynthesis are common. Together, these data show that thiamine acquisition mechanisms used by B. thetaiotaomicron not only are critical for its physiology and fitness but also provide the opportunity to model how other gut microbes may respond to the shifting availability of thiamine in the gut. IMPORTANCE Variation in the ability of gut microbes to transport, synthesize, and compete for vitamin B1 (thiamine) is expected to impact the structure and stability of the microbiota, and ultimately this variation may have both direct and indirect effects on human health. Our study identifies the diverse strategies employed by gut Bacteroidetes to acquire thiamine. We demonstrate how the presence or absence of thiamine biosynthesis or transport dramatically affects the abundance of B. thetaiotaomicron in a competitive environment. This study adds further evidence that altering the presence or concentrations of water-soluble vitamins such as thiamine may be an effective method for manipulating gut community composition. In turn, targeted thiamine delivery could be used therapeutically to alter dysbiotic communities linked to disease. Author Video: An author video summary of this article is available.Zachary A. CostliowPatrick H. DegnanAmerican Society for MicrobiologyarticlecompetitionmicrobiomepnuTthiamine pyrophosphate (TPP)vitamin B1MicrobiologyQR1-502ENmSystems, Vol 2, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	competition microbiome pnuT thiamine pyrophosphate (TPP) vitamin B1 Microbiology QR1-502
spellingShingle	competition microbiome pnuT thiamine pyrophosphate (TPP) vitamin B1 Microbiology QR1-502 Zachary A. Costliow Patrick H. Degnan Thiamine Acquisition Strategies Impact Metabolism and Competition in the Gut Microbe <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
description	ABSTRACT Thiamine (vitamin B1) is an essential cofactor for all organisms. Humans primarily acquire thiamine through their diet, and thiamine deficiencies have adverse neurological effects. However, the role gut microbes play in modulating thiamine availability is poorly understood, and little is known about how thiamine impacts the stability of microbial gut communities. To investigate thiamine’s role in the gut, we utilized the model gut microbe Bacteroides thetaiotaomicron. Transcriptome sequencing (RNA-seq) revealed a global downregulation of thiamine and amino acid biosynthesis, glycolysis, and purine metabolism when thiamine was present. Using genetic mutants with thiamine biosynthesis and transport locus mutations, we determined both systems were critical for growth in thiamine-deficient medium. The defect in the double transport mutant suggests an uncharacterized feedback mechanism between thiamine transport and biosynthesis in B. thetaiotaomicron. Mutant phenotypes were recapitulated during pairwise competitions, reinforcing the importance of encoding versatile thiamine acquisition mechanisms when thiamine concentrations are variable. In addition, liquid chromatography-mass spectrometry (LC-MS) analyses corroborate that exogenous thiamine levels affect the internal thiamine pool of B. thetaiotaomicron. Furthermore, we computationally examined the ability of other gut microbes to acquire thiamine and identified lineage-specific differences in thiamine acquisition strategies. Among the Bacteroidetes, the capacities for both thiamine transport and biosynthesis are common. Together, these data show that thiamine acquisition mechanisms used by B. thetaiotaomicron not only are critical for its physiology and fitness but also provide the opportunity to model how other gut microbes may respond to the shifting availability of thiamine in the gut. IMPORTANCE Variation in the ability of gut microbes to transport, synthesize, and compete for vitamin B1 (thiamine) is expected to impact the structure and stability of the microbiota, and ultimately this variation may have both direct and indirect effects on human health. Our study identifies the diverse strategies employed by gut Bacteroidetes to acquire thiamine. We demonstrate how the presence or absence of thiamine biosynthesis or transport dramatically affects the abundance of B. thetaiotaomicron in a competitive environment. This study adds further evidence that altering the presence or concentrations of water-soluble vitamins such as thiamine may be an effective method for manipulating gut community composition. In turn, targeted thiamine delivery could be used therapeutically to alter dysbiotic communities linked to disease. Author Video: An author video summary of this article is available.
format	article
author	Zachary A. Costliow Patrick H. Degnan
author_facet	Zachary A. Costliow Patrick H. Degnan
author_sort	Zachary A. Costliow
title	Thiamine Acquisition Strategies Impact Metabolism and Competition in the Gut Microbe <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_short	Thiamine Acquisition Strategies Impact Metabolism and Competition in the Gut Microbe <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_full	Thiamine Acquisition Strategies Impact Metabolism and Competition in the Gut Microbe <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_fullStr	Thiamine Acquisition Strategies Impact Metabolism and Competition in the Gut Microbe <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_full_unstemmed	Thiamine Acquisition Strategies Impact Metabolism and Competition in the Gut Microbe <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_sort	thiamine acquisition strategies impact metabolism and competition in the gut microbe <named-content content-type="genus-species">bacteroides thetaiotaomicron</named-content>
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/8f0dc9063eaa45e189acf3a05182d9e9
work_keys_str_mv	AT zacharyacostliow thiamineacquisitionstrategiesimpactmetabolismandcompetitioninthegutmicrobenamedcontentcontenttypegenusspeciesbacteroidesthetaiotaomicronnamedcontent AT patrickhdegnan thiamineacquisitionstrategiesimpactmetabolismandcompetitioninthegutmicrobenamedcontentcontenttypegenusspeciesbacteroidesthetaiotaomicronnamedcontent
_version_	1718376038428311552

Thiamine Acquisition Strategies Impact Metabolism and Competition in the Gut Microbe <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>

Ejemplares similares