Bacteroides ovatus colonization influences the abundance of intestinal short chain fatty acids and neurotransmitters

Thomas D Horvath; Faith D Ihekweazu; Sigmund J Haidacher; Wenly Ruan; Kristen A Engevik; Robert Fultz; Kathleen M Hoch; Ruth Ann Luna; Numan Oezguen; Jennifer K Spinler; Anthony M Haag; James Versalovic; Melinda A Engevik

doi:10.1016/j.isci.2022.104158

Bacteroides ovatus colonization influences the abundance of intestinal short chain fatty acids and neurotransmitters

iScience. 2022 Mar 25;25(5):104158. doi: 10.1016/j.isci.2022.104158. eCollection 2022 May 20.

Authors

Thomas D Horvath^{1

2}, Faith D Ihekweazu^{3

4}, Sigmund J Haidacher^{1

2}, Wenly Ruan^{3

4}, Kristen A Engevik⁵, Robert Fultz⁶, Kathleen M Hoch^{1

2}, Ruth Ann Luna^{1

2}, Numan Oezguen^{1

2}, Jennifer K Spinler^{1

2}, Anthony M Haag^{1

2}, James Versalovic^{1

2}, Melinda A Engevik^{1

7}

Affiliations

¹ Department of Pathology and Immunology, Baylor College of Medicine, Houston, TX, USA.
² Department of Pathology, Texas Children's Hospital, Houston, TX, USA.
³ Department of Pediatrics, Baylor College of Medicine, Houston, TX, USA.
⁴ Section of Gastroenterology, Hepatology, and Nutrition, Texas Children's Hospital, Houston, TX, USA.
⁵ Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, TX, USA.
⁶ Department of Neuroscience, Cell Biology, and Anatomy, University of Texas Medical Branch, Galveston, TX, USA.
⁷ Department of Regenerative Medicine & Cell Biology, Medical University of South Carolina, 173 Ashley Ave, BSB 621, Charleston, SC 29425, USA.

Abstract

Gut microbes can synthesize multiple neuro-active metabolites. We profiled neuro-active compounds produced by the gut commensal Bacteroides ovatus in vitro and in vivo by LC-MS/MS. We found that B. ovatus generates acetic acid, propionic acid, isobutyric acid, and isovaleric acid. In vitro, B. ovatus consumed tryptophan and glutamate and synthesized the neuro-active compounds glutamine and GABA. Consistent with our LC-MS/MS-based in vitro data, we observed elevated levels of acetic acid, propionic acid, isobutyric acid, and isovaleric acid in the intestines of B. ovatus mono-associated mice compared with germ-free controls. B. ovatus mono-association also increased the concentrations of intestinal GABA and decreased the concentrations of tryptophan and glutamine compared with germ-free controls. Computational network analysis revealed unique links between SCFAs, neuro-active compounds, and colonization status. These results highlight connections between microbial colonization and intestinal neurotransmitter concentrations, suggesting that B. ovatus selectively influences the presence of intestinal neurotransmitters.

Keywords: Microbiology; Microbiome; Neuroscience.

Grants and funding

P30 DK123704/DK/NIDDK NIH HHS/United States