Association of intratumoral microbiome diversity with hepatocellular carcinoma prognosis

ABSTRACT The evidence that intratumoral microbiomes, as a rising hallmark of cancer, have a profound impact on cancer phenotypes is increasingly compelling. However, the impact of the composition and diversity of the intratumoral microbiome on the prognosis of patients undergoing surgical resection...

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Main Authors: Fengle Jiang, Yuan Dang, Zheting Zhang, Yanan Yan, Yingchao Wang, Yi Chen, Lihong Chen, Jialiang Zhang, Jingfeng Liu, Jianmin Wang
Format: Article
Language:English
Published: American Society for Microbiology 2025-01-01
Series:mSystems
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Online Access:https://journals.asm.org/doi/10.1128/msystems.00765-24
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author Fengle Jiang
Yuan Dang
Zheting Zhang
Yanan Yan
Yingchao Wang
Yi Chen
Lihong Chen
Jialiang Zhang
Jingfeng Liu
Jianmin Wang
author_facet Fengle Jiang
Yuan Dang
Zheting Zhang
Yanan Yan
Yingchao Wang
Yi Chen
Lihong Chen
Jialiang Zhang
Jingfeng Liu
Jianmin Wang
author_sort Fengle Jiang
collection DOAJ
description ABSTRACT The evidence that intratumoral microbiomes, as a rising hallmark of cancer, have a profound impact on cancer phenotypes is increasingly compelling. However, the impact of the composition and diversity of the intratumoral microbiome on the prognosis of patients undergoing surgical resection for hepatocellular carcinoma (HCC) remains incompletely understood. In this study, we revealed a high abundance of bacteria in the neoplastic tissues. The presence of bacterial lipopolysaccharide and lipoteichoic acid was detected alongside tumor-associated immune cells. By utilizing 16S rRNA gene sequencing, we identified a specific intratumoral microbiome signature that was highly predictive of the prognosis for HCC patients who underwent surgical resection. Specifically, the presence of Intestinimonas, Brachybacterium, and Rothia were identified as independent risk factors for the overall survival of HCC patients who underwent surgical resection.IMPORTANCEAlthough some studies have shown an abundance of bacteria in hepatocellular carcinoma (HCC), there is still limited understanding of the composition and diversity of the intratumoral microbiome that is favorable or adverse to the prognosis of HCC patients. Our results indicated that a greater abundance of bacteria could be observed in the neoplastic tissues than in nonneoplastic tissues. Bacterial cell wall components largely coincided with tumor-associated immune cells. The bacteria in the long overall survival (LOS) group were associated with metabolism and cytokine‒cytokine receptor interaction pathways, while bacteria in the short overall survival (SOS) group were associated with proinflammatory and cell proliferation pathways. Notably, specific taxa could independently predict HCC prognosis. Based on these findings, intratumoral microbiomes facilitate the use of precision medicine in clinical practice.
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publisher American Society for Microbiology
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spelling doaj-art-983c858827774151b1462bc48bad95aa2025-01-21T14:00:28ZengAmerican Society for MicrobiologymSystems2379-50772025-01-0110110.1128/msystems.00765-24Association of intratumoral microbiome diversity with hepatocellular carcinoma prognosisFengle Jiang0Yuan Dang1Zheting Zhang2Yanan Yan3Yingchao Wang4Yi Chen5Lihong Chen6Jialiang Zhang7Jingfeng Liu8Jianmin Wang9Innovation Center for Cancer Research, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, ChinaInnovation Center for Cancer Research, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, ChinaInnovation Center for Cancer Research, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, ChinaInnovation Center for Cancer Research, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, ChinaThe United Innovation of Mengchao Hepatobiliary Technology Key Laboratory of Fujian Province, Mengchao Hepatobiliary Hospital of Fujian Medical University, Fuzhou, ChinaThe United Innovation of Mengchao Hepatobiliary Technology Key Laboratory of Fujian Province, Mengchao Hepatobiliary Hospital of Fujian Medical University, Fuzhou, ChinaThe United Innovation of Mengchao Hepatobiliary Technology Key Laboratory of Fujian Province, Mengchao Hepatobiliary Hospital of Fujian Medical University, Fuzhou, ChinaInnovation Center for Cancer Research, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, ChinaInnovation Center for Cancer Research, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, ChinaInnovation Center for Cancer Research, Clinical Oncology School of Fujian Medical University, Fujian Cancer Hospital, Fuzhou, ChinaABSTRACT The evidence that intratumoral microbiomes, as a rising hallmark of cancer, have a profound impact on cancer phenotypes is increasingly compelling. However, the impact of the composition and diversity of the intratumoral microbiome on the prognosis of patients undergoing surgical resection for hepatocellular carcinoma (HCC) remains incompletely understood. In this study, we revealed a high abundance of bacteria in the neoplastic tissues. The presence of bacterial lipopolysaccharide and lipoteichoic acid was detected alongside tumor-associated immune cells. By utilizing 16S rRNA gene sequencing, we identified a specific intratumoral microbiome signature that was highly predictive of the prognosis for HCC patients who underwent surgical resection. Specifically, the presence of Intestinimonas, Brachybacterium, and Rothia were identified as independent risk factors for the overall survival of HCC patients who underwent surgical resection.IMPORTANCEAlthough some studies have shown an abundance of bacteria in hepatocellular carcinoma (HCC), there is still limited understanding of the composition and diversity of the intratumoral microbiome that is favorable or adverse to the prognosis of HCC patients. Our results indicated that a greater abundance of bacteria could be observed in the neoplastic tissues than in nonneoplastic tissues. Bacterial cell wall components largely coincided with tumor-associated immune cells. The bacteria in the long overall survival (LOS) group were associated with metabolism and cytokine‒cytokine receptor interaction pathways, while bacteria in the short overall survival (SOS) group were associated with proinflammatory and cell proliferation pathways. Notably, specific taxa could independently predict HCC prognosis. Based on these findings, intratumoral microbiomes facilitate the use of precision medicine in clinical practice.https://journals.asm.org/doi/10.1128/msystems.00765-24intratumoral microbiomehepatocellular carcinoma16S rRNA gene sequencingbacterial componentstumor-associated immune cells
spellingShingle Fengle Jiang
Yuan Dang
Zheting Zhang
Yanan Yan
Yingchao Wang
Yi Chen
Lihong Chen
Jialiang Zhang
Jingfeng Liu
Jianmin Wang
Association of intratumoral microbiome diversity with hepatocellular carcinoma prognosis
mSystems
intratumoral microbiome
hepatocellular carcinoma
16S rRNA gene sequencing
bacterial components
tumor-associated immune cells
title Association of intratumoral microbiome diversity with hepatocellular carcinoma prognosis
title_full Association of intratumoral microbiome diversity with hepatocellular carcinoma prognosis
title_fullStr Association of intratumoral microbiome diversity with hepatocellular carcinoma prognosis
title_full_unstemmed Association of intratumoral microbiome diversity with hepatocellular carcinoma prognosis
title_short Association of intratumoral microbiome diversity with hepatocellular carcinoma prognosis
title_sort association of intratumoral microbiome diversity with hepatocellular carcinoma prognosis
topic intratumoral microbiome
hepatocellular carcinoma
16S rRNA gene sequencing
bacterial components
tumor-associated immune cells
url https://journals.asm.org/doi/10.1128/msystems.00765-24
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