Porphyromonas gingivalis aggravates colitis via a gut microbiota-linoleic acid metabolism-Th17/Treg cell balance axis

Lu Jia, Yiyang Jiang, Lili Wu, Jingfei Fu, Juan Du, Zhenhua Luo, Lijia Guo, Junji Xu () and Yi Liu ()
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Lu Jia: Capital Medical University
Yiyang Jiang: Capital Medical University
Lili Wu: Capital Medical University
Jingfei Fu: Capital Medical University
Juan Du: Capital Medical University
Zhenhua Luo: Capital Medical University
Lijia Guo: Capital Medical University
Junji Xu: Capital Medical University
Yi Liu: Capital Medical University

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: Abstract Periodontitis is closely related to inflammatory bowel disease (IBD). An excessive and non-self-limiting immune response to the dysbiotic microbiome characterizes the two. However, the underlying mechanisms that overlap still need to be clarified. We demonstrate that the critical periodontal pathogen Porphyromonas gingivalis (Pg) aggravates intestinal inflammation and Th17/Treg cell imbalance in a gut microbiota-dependent manner. Specifically, metagenomic and metabolomic analyses shows that oral administration of Pg increases levels of the Bacteroides phylum but decreases levels of the Firmicutes, Verrucomicrobia, and Actinobacteria phyla. Nevertheless, it suppresses the linoleic acid (LA) pathway in the gut microbiota, which was the target metabolite that determines the degree of inflammation and functions as an aryl hydrocarbon receptor (AHR) ligand to suppress Th17 differentiation while promoting Treg cell differentiation via the phosphorylation of Stat1 at Ser727. Therapeutically restoring LA levels in colitis mice challenged with Pg exerts anti-colitis effects by decreasing the Th17/Treg cell ratio in an AHR-dependent manner. Our study suggests that Pg aggravates colitis via a gut microbiota-LA metabolism-Th17/Treg cell balance axis, providing a potential therapeutically modifiable target for IBD patients with periodontitis.

Date: 2024
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DOI: 10.1038/s41467-024-45473-y

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