Multiomics analysis reveals gut profiles in patients with different brain tumors

Abstract

Background Numerous close relationships between the gut microbiota and various cancers have been described, and several studies suggest that the gut microbiota can influence the central nervous system (CNS), but the relationship between the intestinal microbiome and brain tumors is unclear. Furthermore, the role of action of the gut microbiota on brain tumors has not been well understood, especially in the CNS, which has been considered an immune-privileged organ due to the presence of the blood-brain barrier. Results In the present work, we systematically compared the gut microbiome and metabolite alterations in patients with a brain tumor, including patients with meningioma (MEG), glioma and brain metastasis (BM), with those of healthy controls (HCs) using faecal metagenomics and metabolomics, and used this in relation to clinical indicators to explore their possible causative mechanisms in the disease. In the disease group, bacterial abundance was altered, showing a significant decrease in Gram-positive bacteria such as Lachnospiraceae and a substantial increase in Gram-negative bacteria such as Enterobacteriaceae, while lipopolysaccharide‒associated pathways were also enriched. Additionally, metabolites were changed: most amino acid and fatty acid metabolites increased, while bile acids (BAs) and carbohydrates decreased. However, the differences in bacteria and metabolites between the disease groups were less than those between the HCs. Furthermore, a variety of immune-related clinical indicators, bacteria, metabolites and pathways were significantly altered in the disease groups. Finally, markers based on bacterial flora and metabolites were effective in differentiating the disease groups from the HCs. Conclusions The multiomics data from this study revealed that dysbiosis and metabolic abnormalities were present in the gut of patients with brain tumors. At the same time, host immune abnormalities may be associated with dysbiosis and may lead to tumour development and progression through inflammatory, immune, and metabolic interactions; these altered microbiome-metabolome-host interactions may help explain the pathogenesis of brain tumors, and provide new ideas for the prevention and treatment of brain tumors. The microbiome and its derived metabolites are a promising noninvasive tool for the accurate detection and differentiation of patients with different brain tumors.