Subspecies Niche Specialization in the Oral Microbiome Is Associated with Nasopharyngeal Carcinoma Risk

ABSTRACT Oral health and changes in the oral microbiome have been associated with both local and systemic cancer. Poor oral hygiene is a known risk factor for nasopharyngeal carcinoma (NPC), a virally associated head and neck cancer endemic to southern China. We explored the relationship between NPC...

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Autores principales:	Justine W. Debelius, Tingting Huang, Yonglin Cai, Alexander Ploner, Donal Barrett, Xiaoying Zhou, Xue Xiao, Yancheng Li, Jian Liao, Yuming Zheng, Guangwu Huang, Hans-Olov Adami, Yi Zeng, Zhe Zhang, Weimin Ye
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	16S sequencing Granulicatella adiacens cancer case-control study microbiome nasopharyngeal carcinoma Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3eb54150230f4eff82d6a792f33370a0
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spelling	oai:doaj.org-article:3eb54150230f4eff82d6a792f33370a02021-12-02T19:46:20ZSubspecies Niche Specialization in the Oral Microbiome Is Associated with Nasopharyngeal Carcinoma Risk10.1128/mSystems.00065-202379-5077https://doaj.org/article/3eb54150230f4eff82d6a792f33370a02020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00065-20https://doaj.org/toc/2379-5077ABSTRACT Oral health and changes in the oral microbiome have been associated with both local and systemic cancer. Poor oral hygiene is a known risk factor for nasopharyngeal carcinoma (NPC), a virally associated head and neck cancer endemic to southern China. We explored the relationship between NPC and the oral microbiome using 16S rRNA sequencing in a study of 499 NPC patients and 495 population-based age and sex frequency-matched controls from an area of endemicity of Southern China. We found a significant reduction in community richness in cases compared to that in controls. Differences in the overall microbial community structure between cases and controls could not be explained by other potential confounders; disease status explained 5 times more variation in the unweighted UniFrac distance than the next most explanatory variable. In feature-based analyses, we identified a pair of coexcluding Granulicatella adiacens amplicon sequence variants (ASVs) which were strongly associated with NPC status and differed by a single nucleotide. The G. adiacens variant an individual carried was also associated with the overall microbial community based on beta diversity. Co-occurrence analysis suggested the two G. adiacens ASVs sit at the center of two coexcluding clusters of closely related organisms. Our results suggest there are differences in the oral microbiomes between NPC patients and healthy controls, and these may be associated with both a loss of microbial diversity and niche specialization among closely related commensals. IMPORTANCE The relationship between oral health and the risk of nasopharyngeal carcinoma (NPC) was previously established. However, the role of oral microbiome has not been evaluated in the disease in a large epidemiological study. This paper clearly establishes a difference in the oral microbiomes between NPC patients and healthy controls which cannot be explained by other confounding factors. It furthermore identifies a pair of closely related coexcluding organisms associated with the disease, highlighting the importance of modern methods for single-nucleotide resolution in 16S rRNA sequence characterization. To the best of our knowledge, this is one of the first examples of cancer-associated niche specialization of the oral microbiome.Justine W. DebeliusTingting HuangYonglin CaiAlexander PlonerDonal BarrettXiaoying ZhouXue XiaoYancheng LiJian LiaoYuming ZhengGuangwu HuangHans-Olov AdamiYi ZengZhe ZhangWeimin YeAmerican Society for Microbiologyarticle16S sequencingGranulicatella adiacenscancercase-control studymicrobiomenasopharyngeal carcinomaMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	16S sequencing Granulicatella adiacens cancer case-control study microbiome nasopharyngeal carcinoma Microbiology QR1-502
spellingShingle	16S sequencing Granulicatella adiacens cancer case-control study microbiome nasopharyngeal carcinoma Microbiology QR1-502 Justine W. Debelius Tingting Huang Yonglin Cai Alexander Ploner Donal Barrett Xiaoying Zhou Xue Xiao Yancheng Li Jian Liao Yuming Zheng Guangwu Huang Hans-Olov Adami Yi Zeng Zhe Zhang Weimin Ye Subspecies Niche Specialization in the Oral Microbiome Is Associated with Nasopharyngeal Carcinoma Risk
description	ABSTRACT Oral health and changes in the oral microbiome have been associated with both local and systemic cancer. Poor oral hygiene is a known risk factor for nasopharyngeal carcinoma (NPC), a virally associated head and neck cancer endemic to southern China. We explored the relationship between NPC and the oral microbiome using 16S rRNA sequencing in a study of 499 NPC patients and 495 population-based age and sex frequency-matched controls from an area of endemicity of Southern China. We found a significant reduction in community richness in cases compared to that in controls. Differences in the overall microbial community structure between cases and controls could not be explained by other potential confounders; disease status explained 5 times more variation in the unweighted UniFrac distance than the next most explanatory variable. In feature-based analyses, we identified a pair of coexcluding Granulicatella adiacens amplicon sequence variants (ASVs) which were strongly associated with NPC status and differed by a single nucleotide. The G. adiacens variant an individual carried was also associated with the overall microbial community based on beta diversity. Co-occurrence analysis suggested the two G. adiacens ASVs sit at the center of two coexcluding clusters of closely related organisms. Our results suggest there are differences in the oral microbiomes between NPC patients and healthy controls, and these may be associated with both a loss of microbial diversity and niche specialization among closely related commensals. IMPORTANCE The relationship between oral health and the risk of nasopharyngeal carcinoma (NPC) was previously established. However, the role of oral microbiome has not been evaluated in the disease in a large epidemiological study. This paper clearly establishes a difference in the oral microbiomes between NPC patients and healthy controls which cannot be explained by other confounding factors. It furthermore identifies a pair of closely related coexcluding organisms associated with the disease, highlighting the importance of modern methods for single-nucleotide resolution in 16S rRNA sequence characterization. To the best of our knowledge, this is one of the first examples of cancer-associated niche specialization of the oral microbiome.
format	article
author	Justine W. Debelius Tingting Huang Yonglin Cai Alexander Ploner Donal Barrett Xiaoying Zhou Xue Xiao Yancheng Li Jian Liao Yuming Zheng Guangwu Huang Hans-Olov Adami Yi Zeng Zhe Zhang Weimin Ye
author_facet	Justine W. Debelius Tingting Huang Yonglin Cai Alexander Ploner Donal Barrett Xiaoying Zhou Xue Xiao Yancheng Li Jian Liao Yuming Zheng Guangwu Huang Hans-Olov Adami Yi Zeng Zhe Zhang Weimin Ye
author_sort	Justine W. Debelius
title	Subspecies Niche Specialization in the Oral Microbiome Is Associated with Nasopharyngeal Carcinoma Risk
title_short	Subspecies Niche Specialization in the Oral Microbiome Is Associated with Nasopharyngeal Carcinoma Risk
title_full	Subspecies Niche Specialization in the Oral Microbiome Is Associated with Nasopharyngeal Carcinoma Risk
title_fullStr	Subspecies Niche Specialization in the Oral Microbiome Is Associated with Nasopharyngeal Carcinoma Risk
title_full_unstemmed	Subspecies Niche Specialization in the Oral Microbiome Is Associated with Nasopharyngeal Carcinoma Risk
title_sort	subspecies niche specialization in the oral microbiome is associated with nasopharyngeal carcinoma risk
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/3eb54150230f4eff82d6a792f33370a0
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Subspecies Niche Specialization in the Oral Microbiome Is Associated with Nasopharyngeal Carcinoma Risk

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