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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| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2021-11-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.745469/full |
| _version_ | 1819290000995385344 |
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| author | Robert Fultz Taylor Ticer Faith D. Ihekweazu Faith D. Ihekweazu Thomas D. Horvath Thomas D. Horvath Sigmund J. Haidacher Sigmund J. Haidacher Kathleen M. Hoch Kathleen M. Hoch Meghna Bajaj Jennifer K. Spinler Jennifer K. Spinler Anthony M. Haag Anthony M. Haag Shelly A. Buffington Melinda A. Engevik |
| author_facet | Robert Fultz Taylor Ticer Faith D. Ihekweazu Faith D. Ihekweazu Thomas D. Horvath Thomas D. Horvath Sigmund J. Haidacher Sigmund J. Haidacher Kathleen M. Hoch Kathleen M. Hoch Meghna Bajaj Jennifer K. Spinler Jennifer K. Spinler Anthony M. Haag Anthony M. Haag Shelly A. Buffington Melinda A. Engevik |
| author_sort | Robert Fultz |
| collection | DOAJ |
| 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 H2O2 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. |
| first_indexed | 2024-12-24T03:15:48Z |
| format | Article |
| id | doaj.art-3f81ecd7e8bc48e2bb3e0901f01bfe38 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-24T03:15:48Z |
| publishDate | 2021-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-3f81ecd7e8bc48e2bb3e0901f01bfe382022-12-21T17:17:38ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-11-011210.3389/fmicb.2021.745469745469Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatusRobert Fultz0Taylor Ticer1Faith D. Ihekweazu2Faith D. Ihekweazu3Thomas D. Horvath4Thomas D. Horvath5Sigmund J. Haidacher6Sigmund J. Haidacher7Kathleen M. Hoch8Kathleen M. Hoch9Meghna Bajaj10Jennifer K. Spinler11Jennifer K. Spinler12Anthony M. Haag13Anthony M. Haag14Shelly A. Buffington15Melinda A. Engevik16Department of Neuroscience, Cell Biology, and Anatomy, University of Texas Medical Branch, Galveston, TX, United StatesDepartment of Regenerative Medicine & Cell Biology, Medical University of South Carolina, Charleston, SC, United StatesDepartment of Pediatrics, Baylor College of Medicine, Houston, TX, United StatesSection of Gastroenterology, Hepatology, and Nutrition, Texas Children’s Hospital, Houston, TX, United StatesDepartment of Pathology and Immunology, Baylor College of Medicine, Houston, TX, United StatesDepartment of Pathology, Texas Children’s Hospital, Houston, TX, United StatesDepartment of Pathology and Immunology, Baylor College of Medicine, Houston, TX, United StatesDepartment of Pathology, Texas Children’s Hospital, Houston, TX, United StatesDepartment of Pathology and Immunology, Baylor College of Medicine, Houston, TX, United StatesDepartment of Pathology, Texas Children’s Hospital, Houston, TX, United StatesDepartment of Chemistry and Physics and Department of Biotechnology, Alcorn State University, Lorman, MS, United StatesDepartment of Pathology and Immunology, Baylor College of Medicine, Houston, TX, United StatesDepartment of Pathology, Texas Children’s Hospital, Houston, TX, United StatesDepartment of Pathology and Immunology, Baylor College of Medicine, Houston, TX, United StatesDepartment of Pathology, Texas Children’s Hospital, Houston, TX, United StatesDepartment of Neuroscience, Cell Biology, and Anatomy, University of Texas Medical Branch, Galveston, TX, United StatesDepartment of Regenerative Medicine & Cell Biology, Medical University of South Carolina, Charleston, SC, United StatesBackground: 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 H2O2 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.745469/fullBacteroidesmetabolismcarbohydratespolysaccharidesintestinecommensal |
| spellingShingle | Robert Fultz Taylor Ticer Faith D. Ihekweazu Faith D. Ihekweazu Thomas D. Horvath Thomas D. Horvath Sigmund J. Haidacher Sigmund J. Haidacher Kathleen M. Hoch Kathleen M. Hoch Meghna Bajaj Jennifer K. Spinler Jennifer K. Spinler Anthony M. Haag Anthony M. Haag Shelly A. Buffington Melinda A. Engevik Unraveling the Metabolic Requirements of the Gut Commensal Bacteroides ovatus Frontiers in Microbiology Bacteroides metabolism carbohydrates polysaccharides intestine commensal |
| 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 | Bacteroides metabolism carbohydrates polysaccharides intestine commensal |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.745469/full |
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