Characteristic alterations of gut microbiota and serum metabolites in patients with chronic tinnitus: a multi-omics analysis

ABSTRACT Chronic tinnitus is a central nervous system disorder. Currently, the effects of gut microbiota on tinnitus remain unexplored. To explore the connection between gut microbiota and tinnitus, we conducted 16S rRNA sequencing of fecal microbiota and serum metabolomic analysis in a cohort of 70...

Full description

Saved in:
Bibliographic Details
Main Authors: Jiang Wang, Jia-Hui Xiang, Xu-Yuan Peng, Min Liu, Le-Jia Sun, Min Zhang, Li-Yuan Zhang, Zhi-Bin Chen, Zheng-Quan Tang, Lei Cheng
Format: Article
Language:English
Published: American Society for Microbiology 2025-01-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.01878-24
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1841556110661648384
author Jiang Wang
Jia-Hui Xiang
Xu-Yuan Peng
Min Liu
Le-Jia Sun
Min Zhang
Li-Yuan Zhang
Zhi-Bin Chen
Zheng-Quan Tang
Lei Cheng
author_facet Jiang Wang
Jia-Hui Xiang
Xu-Yuan Peng
Min Liu
Le-Jia Sun
Min Zhang
Li-Yuan Zhang
Zhi-Bin Chen
Zheng-Quan Tang
Lei Cheng
author_sort Jiang Wang
collection DOAJ
description ABSTRACT Chronic tinnitus is a central nervous system disorder. Currently, the effects of gut microbiota on tinnitus remain unexplored. To explore the connection between gut microbiota and tinnitus, we conducted 16S rRNA sequencing of fecal microbiota and serum metabolomic analysis in a cohort of 70 patients with tinnitus and 30 healthy volunteers. We used the weighted gene co-expression network method to analyze the relationship between the gut microbiota and the serum metabolites. The random forest technique was utilized to select metabolites and gut taxa to construct predictive models. A pronounced gut dysbiosis in the tinnitus group, characterized by reduced bacterial diversity, an increased Firmicutes/Bacteroidetes ratio, and some opportunistic bacteria including Aeromonas and Acinetobacter were enriched. In contrast, some beneficial gut probiotics decreased, including Lactobacillales and Lactobacillaceae. In serum metabolomic analysis, serum metabolic disturbances in tinnitus patients and these differential metabolites were enriched in pathways of neuroinflammation, neurotransmitter activity, and synaptic function. The predictive models exhibited great diagnostic performance, achieving 0.94 (95% CI: 0.85–0.98) and 0.96 (95% CI: 0.86–0.99) in the test set. Our study suggests that changes in gut microbiota could potentially influence the occurrence and chronicity of tinnitus, and exert regulatory effects through changes in serum metabolites. Overall, this research provides new perceptions into the potential role of gut microbiota and serum metabolite in the pathogenesis of tinnitus, and proposes the “gut-brain-ear” concept as a pathomechanism underlying tinnitus, with significant clinical diagnostic implications and therapeutic potential.IMPORTANCETinnitus affects millions of people worldwide. Severe cases may lead to sleep disorders, anxiety, and depression, subsequently impacting patients’ lives and increasing societal healthcare expenditures. However, tinnitus mechanisms are poorly understood, and effective therapeutic interventions are currently lacking. We discovered the gut microbiota and serum metabolomics changes in patients with tinnitus, and provided the potential pathological mechanisms of dysregulated gut flora in chronic tinnitus. We proposed the innovative concept of the “gut-brain-ear axis,” which underscores the exploration of gut microbiota impact on susceptibility to chronic tinnitus through serum metabolic profile modulation. We also reveal novel biomarkers associated with chronic tinnitus, offering a new conceptual framework for further investigations into the susceptibility of patients, potential treatment targets for tinnitus, and assessing patient prognosis. Subsequently, gut microbiota and serum metabolites can be used as molecular markers to assess the susceptibility and prognosis of tinnitus.Furthermore, fecal transplantation may be used to treat tinnitus.
format Article
id doaj-art-a06aa25815d646f3b17b42685626e261
institution Kabale University
issn 2165-0497
language English
publishDate 2025-01-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj-art-a06aa25815d646f3b17b42685626e2612025-01-07T14:05:19ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-01-0113110.1128/spectrum.01878-24Characteristic alterations of gut microbiota and serum metabolites in patients with chronic tinnitus: a multi-omics analysisJiang Wang0Jia-Hui Xiang1Xu-Yuan Peng2Min Liu3Le-Jia Sun4Min Zhang5Li-Yuan Zhang6Zhi-Bin Chen7Zheng-Quan Tang8Lei Cheng9Department of Otorhinolaryngology & Hearing International Jiangsu Ear and Hearing Center, The First Affiliated Hospital, Nanjing Medical University, Nanjing, ChinaDepartment of Breast Surgical Oncology, National Cancer Center & National Clinical Research Center for Cancer, Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, ChinaDepartment of Otorhinolaryngology & Hearing International Jiangsu Ear and Hearing Center, The First Affiliated Hospital, Nanjing Medical University, Nanjing, ChinaDepartment of Otorhinolaryngology & Hearing International Jiangsu Ear and Hearing Center, The First Affiliated Hospital, Nanjing Medical University, Nanjing, ChinaDepartment of General Surgery, The First Affiliated Hospital, Nanjing Medical University, Nanjing, ChinaDepartment of Otorhinolaryngology & Hearing International Jiangsu Ear and Hearing Center, The First Affiliated Hospital, Nanjing Medical University, Nanjing, ChinaDepartment of Otorhinolaryngology & Hearing International Jiangsu Ear and Hearing Center, The First Affiliated Hospital, Nanjing Medical University, Nanjing, ChinaDepartment of Otorhinolaryngology & Hearing International Jiangsu Ear and Hearing Center, The First Affiliated Hospital, Nanjing Medical University, Nanjing, ChinaSchool of Life Sciences, Anhui University, Hefei, ChinaDepartment of Otorhinolaryngology & Hearing International Jiangsu Ear and Hearing Center, The First Affiliated Hospital, Nanjing Medical University, Nanjing, ChinaABSTRACT Chronic tinnitus is a central nervous system disorder. Currently, the effects of gut microbiota on tinnitus remain unexplored. To explore the connection between gut microbiota and tinnitus, we conducted 16S rRNA sequencing of fecal microbiota and serum metabolomic analysis in a cohort of 70 patients with tinnitus and 30 healthy volunteers. We used the weighted gene co-expression network method to analyze the relationship between the gut microbiota and the serum metabolites. The random forest technique was utilized to select metabolites and gut taxa to construct predictive models. A pronounced gut dysbiosis in the tinnitus group, characterized by reduced bacterial diversity, an increased Firmicutes/Bacteroidetes ratio, and some opportunistic bacteria including Aeromonas and Acinetobacter were enriched. In contrast, some beneficial gut probiotics decreased, including Lactobacillales and Lactobacillaceae. In serum metabolomic analysis, serum metabolic disturbances in tinnitus patients and these differential metabolites were enriched in pathways of neuroinflammation, neurotransmitter activity, and synaptic function. The predictive models exhibited great diagnostic performance, achieving 0.94 (95% CI: 0.85–0.98) and 0.96 (95% CI: 0.86–0.99) in the test set. Our study suggests that changes in gut microbiota could potentially influence the occurrence and chronicity of tinnitus, and exert regulatory effects through changes in serum metabolites. Overall, this research provides new perceptions into the potential role of gut microbiota and serum metabolite in the pathogenesis of tinnitus, and proposes the “gut-brain-ear” concept as a pathomechanism underlying tinnitus, with significant clinical diagnostic implications and therapeutic potential.IMPORTANCETinnitus affects millions of people worldwide. Severe cases may lead to sleep disorders, anxiety, and depression, subsequently impacting patients’ lives and increasing societal healthcare expenditures. However, tinnitus mechanisms are poorly understood, and effective therapeutic interventions are currently lacking. We discovered the gut microbiota and serum metabolomics changes in patients with tinnitus, and provided the potential pathological mechanisms of dysregulated gut flora in chronic tinnitus. We proposed the innovative concept of the “gut-brain-ear axis,” which underscores the exploration of gut microbiota impact on susceptibility to chronic tinnitus through serum metabolic profile modulation. We also reveal novel biomarkers associated with chronic tinnitus, offering a new conceptual framework for further investigations into the susceptibility of patients, potential treatment targets for tinnitus, and assessing patient prognosis. Subsequently, gut microbiota and serum metabolites can be used as molecular markers to assess the susceptibility and prognosis of tinnitus.Furthermore, fecal transplantation may be used to treat tinnitus.https://journals.asm.org/doi/10.1128/spectrum.01878-24chronic tinnitusgut microbiotaserum metabolitesgut-brain-ear axismulti-omics analysis
spellingShingle Jiang Wang
Jia-Hui Xiang
Xu-Yuan Peng
Min Liu
Le-Jia Sun
Min Zhang
Li-Yuan Zhang
Zhi-Bin Chen
Zheng-Quan Tang
Lei Cheng
Characteristic alterations of gut microbiota and serum metabolites in patients with chronic tinnitus: a multi-omics analysis
Microbiology Spectrum
chronic tinnitus
gut microbiota
serum metabolites
gut-brain-ear axis
multi-omics analysis
title Characteristic alterations of gut microbiota and serum metabolites in patients with chronic tinnitus: a multi-omics analysis
title_full Characteristic alterations of gut microbiota and serum metabolites in patients with chronic tinnitus: a multi-omics analysis
title_fullStr Characteristic alterations of gut microbiota and serum metabolites in patients with chronic tinnitus: a multi-omics analysis
title_full_unstemmed Characteristic alterations of gut microbiota and serum metabolites in patients with chronic tinnitus: a multi-omics analysis
title_short Characteristic alterations of gut microbiota and serum metabolites in patients with chronic tinnitus: a multi-omics analysis
title_sort characteristic alterations of gut microbiota and serum metabolites in patients with chronic tinnitus a multi omics analysis
topic chronic tinnitus
gut microbiota
serum metabolites
gut-brain-ear axis
multi-omics analysis
url https://journals.asm.org/doi/10.1128/spectrum.01878-24
work_keys_str_mv AT jiangwang characteristicalterationsofgutmicrobiotaandserummetabolitesinpatientswithchronictinnitusamultiomicsanalysis
AT jiahuixiang characteristicalterationsofgutmicrobiotaandserummetabolitesinpatientswithchronictinnitusamultiomicsanalysis
AT xuyuanpeng characteristicalterationsofgutmicrobiotaandserummetabolitesinpatientswithchronictinnitusamultiomicsanalysis
AT minliu characteristicalterationsofgutmicrobiotaandserummetabolitesinpatientswithchronictinnitusamultiomicsanalysis
AT lejiasun characteristicalterationsofgutmicrobiotaandserummetabolitesinpatientswithchronictinnitusamultiomicsanalysis
AT minzhang characteristicalterationsofgutmicrobiotaandserummetabolitesinpatientswithchronictinnitusamultiomicsanalysis
AT liyuanzhang characteristicalterationsofgutmicrobiotaandserummetabolitesinpatientswithchronictinnitusamultiomicsanalysis
AT zhibinchen characteristicalterationsofgutmicrobiotaandserummetabolitesinpatientswithchronictinnitusamultiomicsanalysis
AT zhengquantang characteristicalterationsofgutmicrobiotaandserummetabolitesinpatientswithchronictinnitusamultiomicsanalysis
AT leicheng characteristicalterationsofgutmicrobiotaandserummetabolitesinpatientswithchronictinnitusamultiomicsanalysis