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Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatus

Background: Bacteroidetes are the most common bacterial phylum in the mammalian intestine and the effects of several Bacteroides spp. on multiple facets of host physiology have been previously described. Of the Bacteroides spp., Bacteroides ovatus has recently garnered attention due to its beneficia...

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Autores principales: Fultz, Robert, Ticer, Taylor, Ihekweazu, Faith D., Horvath, Thomas D., Haidacher, Sigmund J., Hoch, Kathleen M., Bajaj, Meghna, Spinler, Jennifer K., Haag, Anthony M., Buffington, Shelly A., Engevik, Melinda A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8656163/
https://www.ncbi.nlm.nih.gov/pubmed/34899632
http://dx.doi.org/10.3389/fmicb.2021.745469
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author Fultz, Robert
Ticer, Taylor
Ihekweazu, Faith D.
Horvath, Thomas D.
Haidacher, Sigmund J.
Hoch, Kathleen M.
Bajaj, Meghna
Spinler, Jennifer K.
Haag, Anthony M.
Buffington, Shelly A.
Engevik, Melinda A.
author_facet Fultz, Robert
Ticer, Taylor
Ihekweazu, Faith D.
Horvath, Thomas D.
Haidacher, Sigmund J.
Hoch, Kathleen M.
Bajaj, Meghna
Spinler, Jennifer K.
Haag, Anthony M.
Buffington, Shelly A.
Engevik, Melinda A.
author_sort Fultz, Robert
collection PubMed
description Background: Bacteroidetes are the most common bacterial phylum in the mammalian intestine and the effects of several Bacteroides spp. on multiple facets of host physiology have been previously described. Of the Bacteroides spp., Bacteroides ovatus has recently garnered attention due to its beneficial effects in the context of intestinal inflammation. In this study, we aimed to examine model host intestinal physiological conditions and dietary modifications to characterize their effects on B. ovatus growth. Methods and Results: Using Biolog phenotypic microarrays, we evaluated 62 primary carbon sources and determined that B. ovatus ATCC 8384 can use the following carbohydrates as primary carbon sources: 10 disaccharides, 4 trisaccharides, 4 polysaccharides, 4 polymers, 3 L-linked sugars, 6 D-linked sugars, 5 amino-sugars, 6 alcohol sugars, and 15 organic acids. Proteomic profiling of B. ovatus bacteria revealed that a significant portion of the B. ovatus proteome contains proteins important for metabolism. Among the proteins, we found glycosyl hydrolase (GH) familes GH2, GH5, GH20, GH 43, GH88, GH92, and GH95. We also identified multiple proteins with antioxidant properties and reasoned that these proteins may support B. ovatus growth in the GI tract. Upon further testing, we showed that B. ovatus grew robustly in various pH, osmolarity, bile, ethanol, and H(2)O(2) concentrations; indicating that B. ovatus is a well-adapted gut microbe. Conclusion: Taken together, we have demonstrated that key host and diet-derived changes in the intestinal environment influence B. ovatus growth. These data provide the framework for future work toward understanding how diet and lifestyle interventions may promote a beneficial environment for B. ovatus growth.
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spelling pubmed-86561632021-12-10 Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatus Fultz, Robert Ticer, Taylor Ihekweazu, Faith D. Horvath, Thomas D. Haidacher, Sigmund J. Hoch, Kathleen M. Bajaj, Meghna Spinler, Jennifer K. Haag, Anthony M. Buffington, Shelly A. Engevik, Melinda A. Front Microbiol Microbiology Background: Bacteroidetes are the most common bacterial phylum in the mammalian intestine and the effects of several Bacteroides spp. on multiple facets of host physiology have been previously described. Of the Bacteroides spp., Bacteroides ovatus has recently garnered attention due to its beneficial effects in the context of intestinal inflammation. In this study, we aimed to examine model host intestinal physiological conditions and dietary modifications to characterize their effects on B. ovatus growth. Methods and Results: Using Biolog phenotypic microarrays, we evaluated 62 primary carbon sources and determined that B. ovatus ATCC 8384 can use the following carbohydrates as primary carbon sources: 10 disaccharides, 4 trisaccharides, 4 polysaccharides, 4 polymers, 3 L-linked sugars, 6 D-linked sugars, 5 amino-sugars, 6 alcohol sugars, and 15 organic acids. Proteomic profiling of B. ovatus bacteria revealed that a significant portion of the B. ovatus proteome contains proteins important for metabolism. Among the proteins, we found glycosyl hydrolase (GH) familes GH2, GH5, GH20, GH 43, GH88, GH92, and GH95. We also identified multiple proteins with antioxidant properties and reasoned that these proteins may support B. ovatus growth in the GI tract. Upon further testing, we showed that B. ovatus grew robustly in various pH, osmolarity, bile, ethanol, and H(2)O(2) concentrations; indicating that B. ovatus is a well-adapted gut microbe. Conclusion: Taken together, we have demonstrated that key host and diet-derived changes in the intestinal environment influence B. ovatus growth. These data provide the framework for future work toward understanding how diet and lifestyle interventions may promote a beneficial environment for B. ovatus growth. Frontiers Media S.A. 2021-11-25 /pmc/articles/PMC8656163/ /pubmed/34899632 http://dx.doi.org/10.3389/fmicb.2021.745469 Text en Copyright © 2021 Fultz, Ticer, Ihekweazu, Horvath, Haidacher, Hoch, Bajaj, Spinler, Haag, Buffington and Engevik. 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
Fultz, Robert
Ticer, Taylor
Ihekweazu, Faith D.
Horvath, Thomas D.
Haidacher, Sigmund J.
Hoch, Kathleen M.
Bajaj, Meghna
Spinler, Jennifer K.
Haag, Anthony M.
Buffington, Shelly A.
Engevik, Melinda A.
Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatus
title Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatus
title_full Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatus
title_fullStr Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatus
title_full_unstemmed Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatus
title_short Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatus
title_sort unraveling the metabolic requirements of the gut commensal bacteroides ovatus
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8656163/
https://www.ncbi.nlm.nih.gov/pubmed/34899632
http://dx.doi.org/10.3389/fmicb.2021.745469
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