Metabolome and microbiome alterations in tongue coating of gastric precancerous lesion patients

ABSTRACT

Objective: This paper seeks to provide mechanistic insight into the pathological transition through the analysis of metabolites and microorganisms in the tongue coating of gastric precancerous lesions (GPL) patients.

Methods: GC-TOF-MS and UHPLC-QE-MS metabolomics, combined with 16S rRNA microbiome techniques, were performed to explore the changes in metabolites and microorganisms in the tongue coating of GPL patients.

Results: When compared with 15 controls, 133 metabolites were found to be differentially expressed in 60 GPL cases, of which could be divided into ten categories. Among them, most of the differentially expressed metabolites identified were lipids or lipid-like molecules. These metabolites were implicated in 6 metabolic pathways including glycine, serine and threonine metabolism, arginine and proline metabolism, sphingolipid metabolism, valine, leucine and isoleucine degradation, arachidonic acid metabolism, and tyrosine metabolism. The relative abundances of Alloprevotella, Solobacterium, Rothia, Eikenella, and Aggregatibacter in the GPL group increased significantly relative to the controls and were associated with lipids and lipid-like molecules, organic nitrogen compounds, organic oxygen compounds, phenylpropanoids and polyketides, and organoheterocyclic compounds, respectively.

Conclusions: Compared with healthy people, the changes of tongue coating metabolites in GPL patients were mainly characterized by alterations in lipid metabolism and were associated with localized changes in the microbiome.

KEYWORDS:

• Gastric precancerous lesion
• tongue coating
• metabolome
• microbiome
• biomarkers

Article highlights

1. GPL may be related to the abundance alterations of Alloprevotella, Solobacterium, Rothia, Eikenella, and Aggregatibacter in tongue coating of patients.

2. The changes of tongue coating metabolites in patients with GPL are caused by the interaction between the human body and the tongue coating microorganisms. The main changes are lipid metabolism, involving sphingolipid metabolism and arachidonic acid metabolism.

3. Differential metabolites and microorganisms in tongue coating may be the potential biomarkers for noninvasive diagnosis of GPL.

Authors’ contributions

Yiming Hao was in charge of the study and wrote the whole manuscript. Yiqin Wang helped with the ideas of the study. Renling Zhang helped with the clinical samples collection. Robert Morris and Feng Cheng helped with the revision of the text and grammar of the whole manuscript. Zhujing Zhu helped with the experimentation. Yifeng Xu helped with the correction of the format of the manuscript. All authors agreed to be accountable for all aspects of the work.

Declaration of interest

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties.

Supplementary material

Supplemental data for this article can be accessed here.

Additional information

Funding

This paper was funded by the National Natural Science Foundation of China (No. 81703982). This work was also supported by Shanghai Biotree Biotech Co. Ltd.