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Gut Microbiota Represent a Major Thermogenic Biomass

Evidence supports various roles for microbial metabolites in the control of multiple aspects of host energy flux including feeding behaviors, digestive efficiency, and energy expenditure, but few studies have quantified the energy utilization of the biomass of the gut microbiota itself. Because gut...

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Autores principales: Riedl, Ruth A, Burnett, Colin M L, Pearson, Nicole A, Reho, John J, Mokadem, Mohamad, Edwards, Robert A, Kindel, Tammy L, Kirby, John R, Grobe, Justin L
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8055641/
https://www.ncbi.nlm.nih.gov/pubmed/33939772
http://dx.doi.org/10.1093/function/zqab019
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author Riedl, Ruth A
Burnett, Colin M L
Pearson, Nicole A
Reho, John J
Mokadem, Mohamad
Edwards, Robert A
Kindel, Tammy L
Kirby, John R
Grobe, Justin L
author_facet Riedl, Ruth A
Burnett, Colin M L
Pearson, Nicole A
Reho, John J
Mokadem, Mohamad
Edwards, Robert A
Kindel, Tammy L
Kirby, John R
Grobe, Justin L
author_sort Riedl, Ruth A
collection PubMed
description Evidence supports various roles for microbial metabolites in the control of multiple aspects of host energy flux including feeding behaviors, digestive efficiency, and energy expenditure, but few studies have quantified the energy utilization of the biomass of the gut microbiota itself. Because gut microbiota exist in an anoxic environment, energy flux is expected to be anaerobic; unfortunately, commonly utilized O(2)/CO(2) respirometry-based approaches are unable to detect anaerobic energy flux. To quantify the contribution of the gut microbial biomass to whole-animal energy flux, we examined the effect of surgical reduction of gut biomass in C57BL/6J mice via cecectomy and assessed energy expenditure using methods sensitive to anaerobic flux, including bomb and direct calorimetry. First, we determined that cecectomy caused an acceleration of weight gain over several months due to a reduction in combined total host plus microbial energy expenditure, as reflected by an increase in energy efficiency (ie, weight gained per calorie absorbed). Second, we determined that under general anesthesia, cecectomy caused immediate changes in heat dissipation that were significantly modified by short-term pretreatment with dietary or pharmaceutical interventions known to modify the microbiome, and confirmed that these effects were undetectable by respirometry. We conclude that while the cecum only contributes approximately 1% of body mass in the mouse, this organ contributes roughly 8% of total resting energy expenditure, that this contribution is predominantly anaerobic, and that the composition and abundance of the cecal microbial contents can significantly alter its contribution to energy flux.
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spelling pubmed-80556412021-04-29 Gut Microbiota Represent a Major Thermogenic Biomass Riedl, Ruth A Burnett, Colin M L Pearson, Nicole A Reho, John J Mokadem, Mohamad Edwards, Robert A Kindel, Tammy L Kirby, John R Grobe, Justin L Function (Oxf) Original Research Article Evidence supports various roles for microbial metabolites in the control of multiple aspects of host energy flux including feeding behaviors, digestive efficiency, and energy expenditure, but few studies have quantified the energy utilization of the biomass of the gut microbiota itself. Because gut microbiota exist in an anoxic environment, energy flux is expected to be anaerobic; unfortunately, commonly utilized O(2)/CO(2) respirometry-based approaches are unable to detect anaerobic energy flux. To quantify the contribution of the gut microbial biomass to whole-animal energy flux, we examined the effect of surgical reduction of gut biomass in C57BL/6J mice via cecectomy and assessed energy expenditure using methods sensitive to anaerobic flux, including bomb and direct calorimetry. First, we determined that cecectomy caused an acceleration of weight gain over several months due to a reduction in combined total host plus microbial energy expenditure, as reflected by an increase in energy efficiency (ie, weight gained per calorie absorbed). Second, we determined that under general anesthesia, cecectomy caused immediate changes in heat dissipation that were significantly modified by short-term pretreatment with dietary or pharmaceutical interventions known to modify the microbiome, and confirmed that these effects were undetectable by respirometry. We conclude that while the cecum only contributes approximately 1% of body mass in the mouse, this organ contributes roughly 8% of total resting energy expenditure, that this contribution is predominantly anaerobic, and that the composition and abundance of the cecal microbial contents can significantly alter its contribution to energy flux. Oxford University Press 2021-04-15 /pmc/articles/PMC8055641/ /pubmed/33939772 http://dx.doi.org/10.1093/function/zqab019 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of American Physiological Society. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research Article
Riedl, Ruth A
Burnett, Colin M L
Pearson, Nicole A
Reho, John J
Mokadem, Mohamad
Edwards, Robert A
Kindel, Tammy L
Kirby, John R
Grobe, Justin L
Gut Microbiota Represent a Major Thermogenic Biomass
title Gut Microbiota Represent a Major Thermogenic Biomass
title_full Gut Microbiota Represent a Major Thermogenic Biomass
title_fullStr Gut Microbiota Represent a Major Thermogenic Biomass
title_full_unstemmed Gut Microbiota Represent a Major Thermogenic Biomass
title_short Gut Microbiota Represent a Major Thermogenic Biomass
title_sort gut microbiota represent a major thermogenic biomass
topic Original Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8055641/
https://www.ncbi.nlm.nih.gov/pubmed/33939772
http://dx.doi.org/10.1093/function/zqab019
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