Metabolic Feedback Inhibition Influences Metabolite Secretion by the Human Gut Symbiont <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>

ABSTRACT Microbial metabolism and trophic interactions between microbes give rise to complex multispecies communities in microbe-host systems. Bacteroides thetaiotaomicron (B. theta) is a human gut symbiont thought to play an important role in maintaining host health. Untargeted nuclear magnetic res...

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Autores principales:	Jennie L. Catlett, Jonathan Catazaro, Mikaela Cashman, Sean Carr, Robert Powers, Myra B. Cohen, Nicole R. Buan
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Bacteroides acetate Bacteroides thetaiotaomicron formate metabolism secretion Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b2b7503509444f518e50860f314d0846
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spelling	oai:doaj.org-article:b2b7503509444f518e50860f314d08462021-12-02T19:46:20ZMetabolic Feedback Inhibition Influences Metabolite Secretion by the Human Gut Symbiont <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>10.1128/mSystems.00252-202379-5077https://doaj.org/article/b2b7503509444f518e50860f314d08462020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00252-20https://doaj.org/toc/2379-5077ABSTRACT Microbial metabolism and trophic interactions between microbes give rise to complex multispecies communities in microbe-host systems. Bacteroides thetaiotaomicron (B. theta) is a human gut symbiont thought to play an important role in maintaining host health. Untargeted nuclear magnetic resonance metabolomics revealed B. theta secretes specific organic acids and amino acids in defined minimal medium. Physiological concentrations of acetate and formate found in the human intestinal tract were shown to cause dose-dependent changes in secretion of metabolites known to play roles in host nutrition and pathogenesis. While secretion fluxes varied, biomass yield was unchanged, suggesting feedback inhibition does not affect metabolic bioenergetics but instead redirects carbon and energy to CO2 and H2. Flux balance analysis modeling showed increased flux through CO2-producing reactions under glucose-limiting growth conditions. The metabolic dynamics observed for B. theta, a keystone symbiont organism, underscores the need for metabolic modeling to complement genomic predictions of microbial metabolism to infer mechanisms of microbe-microbe and microbe-host interactions. IMPORTANCE Bacteroides is a highly abundant taxon in the human gut, and Bacteroides thetaiotaomicron (B. theta) is a ubiquitous human symbiont that colonizes the host early in development and persists throughout its life span. The phenotypic plasticity of keystone organisms such as B. theta is important to understand in order to predict phenotype(s) and metabolic interactions under changing nutrient conditions such as those that occur in complex gut communities. Our study shows B. theta prioritizes energy conservation and suppresses secretion of “overflow metabolites” such as organic acids and amino acids when concentrations of acetate are high. Secreted metabolites, especially amino acids, can be a source of nutrients or signals for the host or other microbes in the community. Our study suggests that when metabolically stressed by acetate, B. theta stops sharing with its ecological partners.Jennie L. CatlettJonathan CatazaroMikaela CashmanSean CarrRobert PowersMyra B. CohenNicole R. BuanAmerican Society for MicrobiologyarticleBacteroidesacetateBacteroides thetaiotaomicronformatemetabolismsecretionMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacteroides acetate Bacteroides thetaiotaomicron formate metabolism secretion Microbiology QR1-502
spellingShingle	Bacteroides acetate Bacteroides thetaiotaomicron formate metabolism secretion Microbiology QR1-502 Jennie L. Catlett Jonathan Catazaro Mikaela Cashman Sean Carr Robert Powers Myra B. Cohen Nicole R. Buan Metabolic Feedback Inhibition Influences Metabolite Secretion by the Human Gut Symbiont <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
description	ABSTRACT Microbial metabolism and trophic interactions between microbes give rise to complex multispecies communities in microbe-host systems. Bacteroides thetaiotaomicron (B. theta) is a human gut symbiont thought to play an important role in maintaining host health. Untargeted nuclear magnetic resonance metabolomics revealed B. theta secretes specific organic acids and amino acids in defined minimal medium. Physiological concentrations of acetate and formate found in the human intestinal tract were shown to cause dose-dependent changes in secretion of metabolites known to play roles in host nutrition and pathogenesis. While secretion fluxes varied, biomass yield was unchanged, suggesting feedback inhibition does not affect metabolic bioenergetics but instead redirects carbon and energy to CO2 and H2. Flux balance analysis modeling showed increased flux through CO2-producing reactions under glucose-limiting growth conditions. The metabolic dynamics observed for B. theta, a keystone symbiont organism, underscores the need for metabolic modeling to complement genomic predictions of microbial metabolism to infer mechanisms of microbe-microbe and microbe-host interactions. IMPORTANCE Bacteroides is a highly abundant taxon in the human gut, and Bacteroides thetaiotaomicron (B. theta) is a ubiquitous human symbiont that colonizes the host early in development and persists throughout its life span. The phenotypic plasticity of keystone organisms such as B. theta is important to understand in order to predict phenotype(s) and metabolic interactions under changing nutrient conditions such as those that occur in complex gut communities. Our study shows B. theta prioritizes energy conservation and suppresses secretion of “overflow metabolites” such as organic acids and amino acids when concentrations of acetate are high. Secreted metabolites, especially amino acids, can be a source of nutrients or signals for the host or other microbes in the community. Our study suggests that when metabolically stressed by acetate, B. theta stops sharing with its ecological partners.
format	article
author	Jennie L. Catlett Jonathan Catazaro Mikaela Cashman Sean Carr Robert Powers Myra B. Cohen Nicole R. Buan
author_facet	Jennie L. Catlett Jonathan Catazaro Mikaela Cashman Sean Carr Robert Powers Myra B. Cohen Nicole R. Buan
author_sort	Jennie L. Catlett
title	Metabolic Feedback Inhibition Influences Metabolite Secretion by the Human Gut Symbiont <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_short	Metabolic Feedback Inhibition Influences Metabolite Secretion by the Human Gut Symbiont <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_full	Metabolic Feedback Inhibition Influences Metabolite Secretion by the Human Gut Symbiont <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_fullStr	Metabolic Feedback Inhibition Influences Metabolite Secretion by the Human Gut Symbiont <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_full_unstemmed	Metabolic Feedback Inhibition Influences Metabolite Secretion by the Human Gut Symbiont <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>
title_sort	metabolic feedback inhibition influences metabolite secretion by the human gut symbiont <named-content content-type="genus-species">bacteroides thetaiotaomicron</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/b2b7503509444f518e50860f314d0846
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Metabolic Feedback Inhibition Influences Metabolite Secretion by the Human Gut Symbiont <named-content content-type="genus-species">Bacteroides thetaiotaomicron</named-content>

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