Gut microbiome and metabolome profiling in coal workers’ pneumoconiosis: potential links to pulmonary function

ABSTRACT Coal workers’ pneumoconiosis (CWP) is a severe occupational disease resulting from prolonged exposure to coal dust. However, its pathogenesis remains elusive, compounded by a lack of early detection markers and effective treatments. Although the impact of gut microbiota on lung diseases is...

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Main Authors: Xiao Yu, Tao Xiong, Lu Yu, Gaisheng Liu, Fan Yang, Xueqin Li, Yangyang Wei, Xiaojing Wang, Shuting Wei, Yi Jiang, Xiaomei Kong, Shouan Ren, Yiwei Shi
Format: Article
Language:English
Published: American Society for Microbiology 2024-11-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.00049-24
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author Xiao Yu
Tao Xiong
Lu Yu
Gaisheng Liu
Fan Yang
Xueqin Li
Yangyang Wei
Xiaojing Wang
Shuting Wei
Yi Jiang
Xiaomei Kong
Shouan Ren
Yiwei Shi
author_facet Xiao Yu
Tao Xiong
Lu Yu
Gaisheng Liu
Fan Yang
Xueqin Li
Yangyang Wei
Xiaojing Wang
Shuting Wei
Yi Jiang
Xiaomei Kong
Shouan Ren
Yiwei Shi
author_sort Xiao Yu
collection DOAJ
description ABSTRACT Coal workers’ pneumoconiosis (CWP) is a severe occupational disease resulting from prolonged exposure to coal dust. However, its pathogenesis remains elusive, compounded by a lack of early detection markers and effective treatments. Although the impact of gut microbiota on lung diseases is acknowledged, its specific role in CWP is unclear. This study aims to explore changes in the gut microbiome and metabolome in CWP, while also assessing the correlation between gut microbes and alterations in lung function. Fecal specimens from 43 CWP patients and 48 dust-exposed workers (DEW) were examined using 16S rRNA gene sequencing for microbiota and liquid chromatography-mass spectrometry for metabolite profiling. We observed similar gut microbial α-diversity but significant differences in flora composition (β-diversity) between patients with CWP and the DEW group. After adjusting for age using multifactorial linear regression analysis (MaAsLin2), the distinct gut microbiome profile in CWP patients revealed an increased presence of pro-inflammatory microorganisms such as Klebsiella and Haemophilus. Furthermore, in CWP patients, alterations in gut microbiota—particularly reduced α-diversity and changes in microbial composition—were significantly correlated with impaired pulmonary function, a relationship not observed in DEW. This underscores the specific impact of gut microbiota on pulmonary health in individuals with CWP. Metabolomic analysis of fecal samples from CWP patients and DEW identified 218 differential metabolites between the two groups, with a predominant increase in metabolites in CWP patients, suggesting enhanced metabolic activity in CWP. Key altered metabolites included various lipids, amino acids, and organic compounds, with silibinin emerging as a potential biomarker. Kyoto Encyclopedia of Genes and Genomes pathway enrichment analysis linked these metabolites to pathways relevant to the development of pulmonary fibrosis. Additionally, studies on the interaction between microbiota and metabolites showed positive correlations between certain bacteria and increased metabolites in CWP, further elucidating the complex interplay in this disease state. Our findings suggest a potential contributory role of gut microbiota in CWP pathogenesis through metabolic regulation, with implications for diagnostic biomarkers and understanding disease mechanisms, warranting further molecular investigation.IMPORTANCEThe findings have significant implications for the early diagnosis and treatment of coal workers’ pneumoconiosis, highlighting the potential of gut microbiota as diagnostic biomarkers. They pave the way for new research into gut microbiota-based therapeutic strategies, potentially focusing on modifying gut microbiota to mitigate disease progression.
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spelling doaj-art-2d7e6fc383d74600b489ef32cf5f360b2025-08-20T02:26:20ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-11-01121110.1128/spectrum.00049-24Gut microbiome and metabolome profiling in coal workers’ pneumoconiosis: potential links to pulmonary functionXiao Yu0Tao Xiong1Lu Yu2Gaisheng Liu3Fan Yang4Xueqin Li5Yangyang Wei6Xiaojing Wang7Shuting Wei8Yi Jiang9Xiaomei Kong10Shouan Ren11Yiwei Shi12NHC Key Laboratory of Pneumoconiosis, Shanxi Key Laboratory of Respiratory Diseases, Department of Pulmonary and Critical Care Medicine, The First Hospital of Shanxi Medical University, Taiyuan, ChinaNHC Key Laboratory of Pneumoconiosis, Shanxi Key Laboratory of Respiratory Diseases, Department of Pulmonary and Critical Care Medicine, The First Hospital of Shanxi Medical University, Taiyuan, ChinaNHC Key Laboratory of Pneumoconiosis, Shanxi Key Laboratory of Respiratory Diseases, Department of Pulmonary and Critical Care Medicine, The First Hospital of Shanxi Medical University, Taiyuan, ChinaQuality Control Office, Xishan Occupational Disease Prevention and Control Institute, Taiyuan, ChinaQuality Control Office, Xishan Occupational Disease Prevention and Control Institute, Taiyuan, ChinaDepartment of Respiratory Medicine, Jincheng General Hospital, Shanxi, ChinaNHC Key Laboratory of Pneumoconiosis, Shanxi Key Laboratory of Respiratory Diseases, Department of Pulmonary and Critical Care Medicine, The First Hospital of Shanxi Medical University, Taiyuan, ChinaNHC Key Laboratory of Pneumoconiosis, Shanxi Key Laboratory of Respiratory Diseases, Department of Pulmonary and Critical Care Medicine, The First Hospital of Shanxi Medical University, Taiyuan, ChinaNHC Key Laboratory of Pneumoconiosis, Shanxi Key Laboratory of Respiratory Diseases, Department of Pulmonary and Critical Care Medicine, The First Hospital of Shanxi Medical University, Taiyuan, ChinaNHC Key Laboratory of Pneumoconiosis, Shanxi Key Laboratory of Respiratory Diseases, Department of Pulmonary and Critical Care Medicine, The First Hospital of Shanxi Medical University, Taiyuan, ChinaNHC Key Laboratory of Pneumoconiosis, Shanxi Key Laboratory of Respiratory Diseases, Department of Pulmonary and Critical Care Medicine, The First Hospital of Shanxi Medical University, Taiyuan, ChinaNHC Key Laboratory of Pneumoconiosis, Shanxi Key Laboratory of Respiratory Diseases, Department of Pulmonary and Critical Care Medicine, The First Hospital of Shanxi Medical University, Taiyuan, ChinaNHC Key Laboratory of Pneumoconiosis, Shanxi Key Laboratory of Respiratory Diseases, Department of Pulmonary and Critical Care Medicine, The First Hospital of Shanxi Medical University, Taiyuan, ChinaABSTRACT Coal workers’ pneumoconiosis (CWP) is a severe occupational disease resulting from prolonged exposure to coal dust. However, its pathogenesis remains elusive, compounded by a lack of early detection markers and effective treatments. Although the impact of gut microbiota on lung diseases is acknowledged, its specific role in CWP is unclear. This study aims to explore changes in the gut microbiome and metabolome in CWP, while also assessing the correlation between gut microbes and alterations in lung function. Fecal specimens from 43 CWP patients and 48 dust-exposed workers (DEW) were examined using 16S rRNA gene sequencing for microbiota and liquid chromatography-mass spectrometry for metabolite profiling. We observed similar gut microbial α-diversity but significant differences in flora composition (β-diversity) between patients with CWP and the DEW group. After adjusting for age using multifactorial linear regression analysis (MaAsLin2), the distinct gut microbiome profile in CWP patients revealed an increased presence of pro-inflammatory microorganisms such as Klebsiella and Haemophilus. Furthermore, in CWP patients, alterations in gut microbiota—particularly reduced α-diversity and changes in microbial composition—were significantly correlated with impaired pulmonary function, a relationship not observed in DEW. This underscores the specific impact of gut microbiota on pulmonary health in individuals with CWP. Metabolomic analysis of fecal samples from CWP patients and DEW identified 218 differential metabolites between the two groups, with a predominant increase in metabolites in CWP patients, suggesting enhanced metabolic activity in CWP. Key altered metabolites included various lipids, amino acids, and organic compounds, with silibinin emerging as a potential biomarker. Kyoto Encyclopedia of Genes and Genomes pathway enrichment analysis linked these metabolites to pathways relevant to the development of pulmonary fibrosis. Additionally, studies on the interaction between microbiota and metabolites showed positive correlations between certain bacteria and increased metabolites in CWP, further elucidating the complex interplay in this disease state. Our findings suggest a potential contributory role of gut microbiota in CWP pathogenesis through metabolic regulation, with implications for diagnostic biomarkers and understanding disease mechanisms, warranting further molecular investigation.IMPORTANCEThe findings have significant implications for the early diagnosis and treatment of coal workers’ pneumoconiosis, highlighting the potential of gut microbiota as diagnostic biomarkers. They pave the way for new research into gut microbiota-based therapeutic strategies, potentially focusing on modifying gut microbiota to mitigate disease progression.https://journals.asm.org/doi/10.1128/spectrum.00049-24CWP16S rRNA sequencinggut microbiotaLC-MSfecal metabolomepulmonary function
spellingShingle Xiao Yu
Tao Xiong
Lu Yu
Gaisheng Liu
Fan Yang
Xueqin Li
Yangyang Wei
Xiaojing Wang
Shuting Wei
Yi Jiang
Xiaomei Kong
Shouan Ren
Yiwei Shi
Gut microbiome and metabolome profiling in coal workers’ pneumoconiosis: potential links to pulmonary function
Microbiology Spectrum
CWP
16S rRNA sequencing
gut microbiota
LC-MS
fecal metabolome
pulmonary function
title Gut microbiome and metabolome profiling in coal workers’ pneumoconiosis: potential links to pulmonary function
title_full Gut microbiome and metabolome profiling in coal workers’ pneumoconiosis: potential links to pulmonary function
title_fullStr Gut microbiome and metabolome profiling in coal workers’ pneumoconiosis: potential links to pulmonary function
title_full_unstemmed Gut microbiome and metabolome profiling in coal workers’ pneumoconiosis: potential links to pulmonary function
title_short Gut microbiome and metabolome profiling in coal workers’ pneumoconiosis: potential links to pulmonary function
title_sort gut microbiome and metabolome profiling in coal workers pneumoconiosis potential links to pulmonary function
topic CWP
16S rRNA sequencing
gut microbiota
LC-MS
fecal metabolome
pulmonary function
url https://journals.asm.org/doi/10.1128/spectrum.00049-24
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