A novel interplay between bacteria and metabolites in different early-stage lung cancer: an integrated microbiome and metabolome analysis
BackgroundThe carcinogenesis mechanism of early-stage lung cancer (ESLC) remains unclear. Microbial dysbiosis is closely related to tumor development. This study aimed to analyze the relationship between microbiota dysbiosis in ESLC.MethodsWe investigated a total of 108 surgical specimens of lung no...
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Frontiers Media S.A.
2025-01-01
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| Series: | Frontiers in Oncology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fonc.2024.1492571/full |
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| author | Xiaoqian Zhai Xiaoqian Zhai Dongqi Lin Dongqi Lin Yi Shen Yi Shen Ni Zhai Fan Yu Fan Yu Jiabi Zhang Yiyun Lin Yuqing Wang Qinghua Zhou Qinghua Zhou Xi Zheng Xi Zheng |
| author_facet | Xiaoqian Zhai Xiaoqian Zhai Dongqi Lin Dongqi Lin Yi Shen Yi Shen Ni Zhai Fan Yu Fan Yu Jiabi Zhang Yiyun Lin Yuqing Wang Qinghua Zhou Qinghua Zhou Xi Zheng Xi Zheng |
| author_sort | Xiaoqian Zhai |
| collection | DOAJ |
| description | BackgroundThe carcinogenesis mechanism of early-stage lung cancer (ESLC) remains unclear. Microbial dysbiosis is closely related to tumor development. This study aimed to analyze the relationship between microbiota dysbiosis in ESLC.MethodsWe investigated a total of 108 surgical specimens of lung nodules, including ground glass nodules (GGN) diagnosed as lung adenocarcinoma (n = 25), solid nodules (SN) diagnosed as lung adenocarcinoma (n = 27), lung squamous carcinoma (LUSC) presenting as solid nodules (n = 26), and benign pulmonary nodules (BPD) (n = 30) that were collected. 16S rDNA amplicon sequencing and non-targeted metabolomics analysis were performed in all of the specimens.ResultsWe found a significantly lower microbiota richness in SN than in the GGN and LUSC. Ralstonia may be an important flora promoting the development of early lung adenocarcinoma, while Feacalibacterium and Blautia play a protective role in the progression of GGN to SN. Akkermansia, Escherichia-shigella, and Klebsiella exhibited high abundance in early lung squamous carcinoma. Compared with BPD, the differential metabolites of both early adenocarcinomas (SN and GGN) are mainly involved in energy metabolic pathways, while early LUSC is mainly involved in glutathione metabolism, producing and maintaining high levels of intracellular redox homeostasis. A correlation analysis revealed that different microbiota in GGN may function in energy metabolism via N-acetyl-1-aspartylglutamic acid (NAAG) when compared to BPD, while creatine and N-acetylmethionine were the main relevant molecules for the function of differential microbiota in LUSC.ConclusionOur study identified that early-stage lung adenocarcinoma and squamous carcinoma differ in microbial composition and metabolic status. Ralstonia may be an important flora promoting the development of early lung adenocarcinoma, while Feacalibacterium and Blautia play a protective role in the progression of GGN to SN. Conversely, Akkermansia, Escherichia-shigella, and Klebsiella exhibited high abundance in early lung squamous carcinoma. The metabolites of both early adenocarcinomas (SN and GGN) are mainly involved in energy metabolic pathways, while early LUSC is mainly involved in glutathione metabolism. Our study provides new insights into the carcinogenesis of ESLC. |
| format | Article |
| id | doaj-art-9ed47f8fbefe4c95beb8e3294552ff5d |
| institution | Kabale University |
| issn | 2234-943X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Oncology |
| spelling | doaj-art-9ed47f8fbefe4c95beb8e3294552ff5d2025-01-07T05:23:59ZengFrontiers Media S.A.Frontiers in Oncology2234-943X2025-01-011410.3389/fonc.2024.14925711492571A novel interplay between bacteria and metabolites in different early-stage lung cancer: an integrated microbiome and metabolome analysisXiaoqian Zhai0Xiaoqian Zhai1Dongqi Lin2Dongqi Lin3Yi Shen4Yi Shen5Ni Zhai6Fan Yu7Fan Yu8Jiabi Zhang9Yiyun Lin10Yuqing Wang11Qinghua Zhou12Qinghua Zhou13Xi Zheng14Xi Zheng15Department of Medical Oncology, Cancer Center, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaLung Cancer Center, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaLung Cancer Center, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Thoracic Surgery, West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, Sichuan, ChinaNeurosurgery Intensive Care Unit, The 987th Hospital of the Joint Logistics Support Force of the Chinese People's Liberation Army, Baoji, Shanxi, ChinaLung Cancer Center, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Nutrition and Integrative Physiology, College of Health, University of Utah, Salt Lake City, UT, United StatesGraduate School of Biomedical Sciences, MD Anderson Cancer Center UT Health, Houston, TX, United StatesGraduate School of Biomedical Sciences, Baylor College of Medicine, Houston, TX, United StatesLung Cancer Center, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaLung Cancer Center, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaDepartment of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan, ChinaBackgroundThe carcinogenesis mechanism of early-stage lung cancer (ESLC) remains unclear. Microbial dysbiosis is closely related to tumor development. This study aimed to analyze the relationship between microbiota dysbiosis in ESLC.MethodsWe investigated a total of 108 surgical specimens of lung nodules, including ground glass nodules (GGN) diagnosed as lung adenocarcinoma (n = 25), solid nodules (SN) diagnosed as lung adenocarcinoma (n = 27), lung squamous carcinoma (LUSC) presenting as solid nodules (n = 26), and benign pulmonary nodules (BPD) (n = 30) that were collected. 16S rDNA amplicon sequencing and non-targeted metabolomics analysis were performed in all of the specimens.ResultsWe found a significantly lower microbiota richness in SN than in the GGN and LUSC. Ralstonia may be an important flora promoting the development of early lung adenocarcinoma, while Feacalibacterium and Blautia play a protective role in the progression of GGN to SN. Akkermansia, Escherichia-shigella, and Klebsiella exhibited high abundance in early lung squamous carcinoma. Compared with BPD, the differential metabolites of both early adenocarcinomas (SN and GGN) are mainly involved in energy metabolic pathways, while early LUSC is mainly involved in glutathione metabolism, producing and maintaining high levels of intracellular redox homeostasis. A correlation analysis revealed that different microbiota in GGN may function in energy metabolism via N-acetyl-1-aspartylglutamic acid (NAAG) when compared to BPD, while creatine and N-acetylmethionine were the main relevant molecules for the function of differential microbiota in LUSC.ConclusionOur study identified that early-stage lung adenocarcinoma and squamous carcinoma differ in microbial composition and metabolic status. Ralstonia may be an important flora promoting the development of early lung adenocarcinoma, while Feacalibacterium and Blautia play a protective role in the progression of GGN to SN. Conversely, Akkermansia, Escherichia-shigella, and Klebsiella exhibited high abundance in early lung squamous carcinoma. The metabolites of both early adenocarcinomas (SN and GGN) are mainly involved in energy metabolic pathways, while early LUSC is mainly involved in glutathione metabolism. Our study provides new insights into the carcinogenesis of ESLC.https://www.frontiersin.org/articles/10.3389/fonc.2024.1492571/fullearly-stage lung cancermicrobiomemetabolomecorrelation analysiscarcinogenesis |
| spellingShingle | Xiaoqian Zhai Xiaoqian Zhai Dongqi Lin Dongqi Lin Yi Shen Yi Shen Ni Zhai Fan Yu Fan Yu Jiabi Zhang Yiyun Lin Yuqing Wang Qinghua Zhou Qinghua Zhou Xi Zheng Xi Zheng A novel interplay between bacteria and metabolites in different early-stage lung cancer: an integrated microbiome and metabolome analysis Frontiers in Oncology early-stage lung cancer microbiome metabolome correlation analysis carcinogenesis |
| title | A novel interplay between bacteria and metabolites in different early-stage lung cancer: an integrated microbiome and metabolome analysis |
| title_full | A novel interplay between bacteria and metabolites in different early-stage lung cancer: an integrated microbiome and metabolome analysis |
| title_fullStr | A novel interplay between bacteria and metabolites in different early-stage lung cancer: an integrated microbiome and metabolome analysis |
| title_full_unstemmed | A novel interplay between bacteria and metabolites in different early-stage lung cancer: an integrated microbiome and metabolome analysis |
| title_short | A novel interplay between bacteria and metabolites in different early-stage lung cancer: an integrated microbiome and metabolome analysis |
| title_sort | novel interplay between bacteria and metabolites in different early stage lung cancer an integrated microbiome and metabolome analysis |
| topic | early-stage lung cancer microbiome metabolome correlation analysis carcinogenesis |
| url | https://www.frontiersin.org/articles/10.3389/fonc.2024.1492571/full |
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