Long-read sequencing revealed alterations of microbial relationship between tongue coating and gastric mucosa in patients with gastric intestinal metaplasia

Abstract

Abnormalities of microbiota in tongue coating (TC) are associated with gastric cancer, however, the correlation between microbiota colonizing in TC and in gastric mucosa (GM) and their roles in the development of gastric cancer remain poorly understood. In this study, using long-read sequencing, we profiled the microbiota in both TC and GM from 44 patients with the precancerous gastric intestinal metaplasia (GIM) and 28 matched controls who were rapid urease test (RUT)-negative and had with non-symptomatic chronic superficial gastritis. While no significant difference in diversity of microbiota in either TC or GM was observed between GIM patients and the controls, the distribution of bacteria (operational taxonomic units, OTUs) shared by TC and GM was significantly different between GIM patients and the controls as well as between RUT-positive and RUT-negative GIM patients. LEfSe (Linear discriminant analysis effect size) identified TC Prevotella melaninogenica and three GM Helicobacter species (i.e., H. pylori, H. pylori XZ274, and H. pylori 83) that were enriched in GIM patients, suggesting a potential role of Hp infection in the development of GIM. In RUT-negative GIM patients, gastric Veillonella, Pseudonocardia, and Mesorhizobium were enriched. The commensal network between TC and GM was more complex in patients with GIM than that in controls, and more closely correlated in RUT-positive than in RUT-negative GIM patients. Consistent with the known contribution of H. pylori to lower values of PG-I/PG-II, the serum ratio of PG-I to PG-II was found negatively correlated with the three gastric Helicobacter species (H. pylori, H. pylori XZ274, and H. pylori 83) in RUT-negative GIM patients and negatively correlated with two TC species (Fusobacterium nucleatum subsp. nucleatum and Campylobacter showae) in RUT-positive GIM patients. In summary, the oral and gastric commensal linkage as well as H. pylori infection were promoted in GIM.