Tissue-resident microbiota signature in nasopharyngeal carcinoma
Abstract Background Emerging evidence reveals that microbiota plays a crucial role in multiple cancers. Nasopharyngeal carcinoma (NPC) tissues harbour microbiota, highlighting the need to investigate the clinical implications of tissue-resident microbiota in the development of NPC. Here, we aim to c...
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BMC
2025-05-01
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| Online Access: | https://doi.org/10.1186/s40168-025-02114-w |
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| author | Xi-Rong Tan Han Qiao Ying-Qing Li Wei Jiang Sheng-Yan Huang Sha Gong Wen-Fei Li Ling-Long Tang Guan-Qun Zhou Ye-Lin Liang Hui Li Qing-Mei He Jie-Wen Bai Ming-Liang Ye Jing-Yun Wang Sai-Wei Huang Jun-Yan Li Chun-Qiao Gan Ying-Qin Li Yin Zhao Ying Sun Jun Ma Na Liu |
| author_facet | Xi-Rong Tan Han Qiao Ying-Qing Li Wei Jiang Sheng-Yan Huang Sha Gong Wen-Fei Li Ling-Long Tang Guan-Qun Zhou Ye-Lin Liang Hui Li Qing-Mei He Jie-Wen Bai Ming-Liang Ye Jing-Yun Wang Sai-Wei Huang Jun-Yan Li Chun-Qiao Gan Ying-Qin Li Yin Zhao Ying Sun Jun Ma Na Liu |
| author_sort | Xi-Rong Tan |
| collection | DOAJ |
| description | Abstract Background Emerging evidence reveals that microbiota plays a crucial role in multiple cancers. Nasopharyngeal carcinoma (NPC) tissues harbour microbiota, highlighting the need to investigate the clinical implications of tissue-resident microbiota in the development of NPC. Here, we aim to clarify the specific profile of tissue-resident microbiota and its influence on NPC outcomes. Results This retrospective study included 491 NPC patients from Sun Yat-sen University Cancer Center (Guangzhou, China) and the Affiliated Hospital of Guilin Medical College (Guilin, China). We profiled the microbial composition of 343 NPC and 36 normal nasopharyngeal tissues through sequencing of the genes encoding the 16S rRNA subunit of bacterial ribosomes. There were significant differences in microbial composition, alpha diversity (Shannon index, P = 0.007; Simpson index, P = 0.036), and beta diversity (Bray–Curtis distance: R 2 = 0.016, F = 5.187, P = 0.001; unweighted UniFrac distance: R 2 = 0.017, F = 5.373, P = 0.001) between NPC and normal nasopharyngeal tissues. A bacterial signature comprising four risk bacterial genera, including Bacteroides, Alloprevotella, Parvimonas, and Dialister, was constructed in the training cohort (n = 171). Patients in the high-risk group had shorter disease-free (HR 2.80, 95% CI 1.51–5.18, P < 0.001), distant metastasis-free (HR 4.00, 95% CI 1.77–9.01, P < 0.001), and overall survival (HR 3.45, 95% CI 1.77–6.72, P < 0.001) than those of patients in the low-risk group. Similar results were yielded in the internal validation (n = 172) and external validation (n = 148) cohorts. Integrated multi-omics analysis revealed that NPC tissues harbouring abundant risk bacteria were characterised by deficient immune infiltration, which was verified by multiplex immunohistochemistry. Conclusions This study developed and validated the applicability of a four-bacteria signature as a prognostic tool for NPC prognostication. Integrated multi-omics analysis further uncovered that the tumour immune microenvironment was perturbed by tissue-resident microbiota, which might pave the way towards the era of microbiota-targeted precision medicine for NPC. Video Abstract |
| format | Article |
| id | doaj-art-c6b268cbe3d94fd5aeae949ebd132e83 |
| institution | OA Journals |
| issn | 2049-2618 |
| language | English |
| publishDate | 2025-05-01 |
| publisher | BMC |
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| series | Microbiome |
| spelling | doaj-art-c6b268cbe3d94fd5aeae949ebd132e832025-08-20T02:25:12ZengBMCMicrobiome2049-26182025-05-0113111510.1186/s40168-025-02114-wTissue-resident microbiota signature in nasopharyngeal carcinomaXi-Rong Tan0Han Qiao1Ying-Qing Li2Wei Jiang3Sheng-Yan Huang4Sha Gong5Wen-Fei Li6Ling-Long Tang7Guan-Qun Zhou8Ye-Lin Liang9Hui Li10Qing-Mei He11Jie-Wen Bai12Ming-Liang Ye13Jing-Yun Wang14Sai-Wei Huang15Jun-Yan Li16Chun-Qiao Gan17Ying-Qin Li18Yin Zhao19Ying Sun20Jun Ma21Na Liu22Department of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Out-Patient, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Radiation Oncology, Affiliated Hospital of Guilin Medical UniversityDepartment of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Radiation Oncology, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Radiation Oncology, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Radiation Oncology, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Radiation Oncology, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterZhongshan School of Medicine, Sun Yat-Sen UniversityDepartment of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Radiation Oncology, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Radiation Oncology, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Radiation Oncology, Affiliated Hospital of Guilin Medical UniversityDepartment of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Radiation Oncology, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Radiation Oncology, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterDepartment of Experimental Research, State Key Laboratory of Oncology in South China, Guangdong Key Laboratory of Nasopharyngeal Carcinoma Diagnosis and Therapy, Guangdong Provincial Clinical Research Center for Cancer, Sun Yat-sen University Cancer CenterAbstract Background Emerging evidence reveals that microbiota plays a crucial role in multiple cancers. Nasopharyngeal carcinoma (NPC) tissues harbour microbiota, highlighting the need to investigate the clinical implications of tissue-resident microbiota in the development of NPC. Here, we aim to clarify the specific profile of tissue-resident microbiota and its influence on NPC outcomes. Results This retrospective study included 491 NPC patients from Sun Yat-sen University Cancer Center (Guangzhou, China) and the Affiliated Hospital of Guilin Medical College (Guilin, China). We profiled the microbial composition of 343 NPC and 36 normal nasopharyngeal tissues through sequencing of the genes encoding the 16S rRNA subunit of bacterial ribosomes. There were significant differences in microbial composition, alpha diversity (Shannon index, P = 0.007; Simpson index, P = 0.036), and beta diversity (Bray–Curtis distance: R 2 = 0.016, F = 5.187, P = 0.001; unweighted UniFrac distance: R 2 = 0.017, F = 5.373, P = 0.001) between NPC and normal nasopharyngeal tissues. A bacterial signature comprising four risk bacterial genera, including Bacteroides, Alloprevotella, Parvimonas, and Dialister, was constructed in the training cohort (n = 171). Patients in the high-risk group had shorter disease-free (HR 2.80, 95% CI 1.51–5.18, P < 0.001), distant metastasis-free (HR 4.00, 95% CI 1.77–9.01, P < 0.001), and overall survival (HR 3.45, 95% CI 1.77–6.72, P < 0.001) than those of patients in the low-risk group. Similar results were yielded in the internal validation (n = 172) and external validation (n = 148) cohorts. Integrated multi-omics analysis revealed that NPC tissues harbouring abundant risk bacteria were characterised by deficient immune infiltration, which was verified by multiplex immunohistochemistry. Conclusions This study developed and validated the applicability of a four-bacteria signature as a prognostic tool for NPC prognostication. Integrated multi-omics analysis further uncovered that the tumour immune microenvironment was perturbed by tissue-resident microbiota, which might pave the way towards the era of microbiota-targeted precision medicine for NPC. Video Abstracthttps://doi.org/10.1186/s40168-025-02114-wNasopharyngeal carcinomaPrognosisMicrobiota signatureBacteriaTumour microenvironment |
| spellingShingle | Xi-Rong Tan Han Qiao Ying-Qing Li Wei Jiang Sheng-Yan Huang Sha Gong Wen-Fei Li Ling-Long Tang Guan-Qun Zhou Ye-Lin Liang Hui Li Qing-Mei He Jie-Wen Bai Ming-Liang Ye Jing-Yun Wang Sai-Wei Huang Jun-Yan Li Chun-Qiao Gan Ying-Qin Li Yin Zhao Ying Sun Jun Ma Na Liu Tissue-resident microbiota signature in nasopharyngeal carcinoma Microbiome Nasopharyngeal carcinoma Prognosis Microbiota signature Bacteria Tumour microenvironment |
| title | Tissue-resident microbiota signature in nasopharyngeal carcinoma |
| title_full | Tissue-resident microbiota signature in nasopharyngeal carcinoma |
| title_fullStr | Tissue-resident microbiota signature in nasopharyngeal carcinoma |
| title_full_unstemmed | Tissue-resident microbiota signature in nasopharyngeal carcinoma |
| title_short | Tissue-resident microbiota signature in nasopharyngeal carcinoma |
| title_sort | tissue resident microbiota signature in nasopharyngeal carcinoma |
| topic | Nasopharyngeal carcinoma Prognosis Microbiota signature Bacteria Tumour microenvironment |
| url | https://doi.org/10.1186/s40168-025-02114-w |
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