Oral Microbiome Alterations Associated with Early Childhood Caries Highlight the Importance of Carbohydrate Metabolic Activities

Dental caries is a highly prevalent oral disease that can lead to severe dental damage and may greatly compromise the quality of life of the affected individuals. Previous studies, including those based on 16S rRNA gene, have revealed that the oral microbiota plays a prominent role in development of...

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Main Authors: Yuan Wang, Sa Wang, Chunyan Wu, Xi Chen, Zhuhui Duan, Qian Xu, Wen Jiang, Lei Xu, Tingting Wang, Lingkai Su, Ying Wang, Yadong Chen, Jie Zhang, Yun Huang, Suman Tong, Cheng Zhou, Shuli Deng, Nan Qin
Format: Article
Language:English
Published: American Society for Microbiology 2019-11-01
Series:mSystems
Subjects:
Online Access:https://doi.org/10.1128/mSystems.00450-19
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spelling doaj-d9effcb441fd4c32bb81cd869cc4adef2020-11-25T01:28:52ZengAmerican Society for MicrobiologymSystems2379-50772019-11-0146e00450-1910.1128/mSystems.00450-19Oral Microbiome Alterations Associated with Early Childhood Caries Highlight the Importance of Carbohydrate Metabolic ActivitiesYuan WangSa WangChunyan WuXi ChenZhuhui DuanQian XuWen JiangLei XuTingting WangLingkai SuYing WangYadong ChenJie ZhangYun HuangSuman TongCheng ZhouShuli DengNan QinDental caries is a highly prevalent oral disease that can lead to severe dental damage and may greatly compromise the quality of life of the affected individuals. Previous studies, including those based on 16S rRNA gene, have revealed that the oral microbiota plays a prominent role in development of the disease. But the approach of those studies was limited in analyzing several key microbiome traits, including species- or strain-level composition and functional profile. Here, we performed metagenomic analyses for a cohort of preschool children with or without caries. Our results showed that caries was associated with extensive microbiota differences at various taxonomic and functional levels. Some caries-associated species had not been previously reported, some of which may have significant clinical implications. A microbiome gene catalogue from children with caries was constructed for the first time. The results demonstrated that caries is associated with alterations of the oral microbiome, including changes in microbial composition and metabolic functional profile.Globally, dental caries is the most prevalent chronic oral disease and affects roughly half of all children. The aim of this report was to use metagenomic analyses to investigate the relationship between the oral microbiome and caries in preschool children. A total of 25 preschoolers, aged 3 to 5 years old with severe early childhood caries (ECC), and 19 age-matched, caries-free children as controls were recruited. Saliva samples were collected from the participants and were subjected to metagenomic analyses, whereby the oral microbial communities were investigated. The metagenomic analyses revealed substantial microbiota differences between the two groups, indicating apparent shifts of the oral microbiome present in the ECC group. At the species level, the ECC-enriched microbes included Prevotella amnii, Shuttleworthia satelles, Olsenella uli, and Anaeroglobus geminatus. Interestingly, Actinomyces odontolyticus and Actinomyces graevenitzii exhibited apparent differences at the strain level but not the species level between the ECC and control groups. Functional examination showed that the ECC group displayed extensive alterations in metabolic genes/pathways/modules, including enriched functions in sugar metabolism. Finally, an SVM (support vector machine) classifier comprising seven species was developed and generated a moderately good performance in predicting caries onset (area under the receiver operating characteristic curve [AUC] = 78.33%). Together, these findings indicate that caries is associated with considerable changes in the oral microbiome, some of which can potentially be exploited as therapeutic targets or diagnostic markers. (This study has been registered at ClinicalTrials.gov under registration no. NCT02341352.)https://doi.org/10.1128/mSystems.00450-19early childhood cariesmetagenomicsoral microbiomefunctional profilepreschool children
collection DOAJ
language English
format Article
sources DOAJ
author Yuan Wang
Sa Wang
Chunyan Wu
Xi Chen
Zhuhui Duan
Qian Xu
Wen Jiang
Lei Xu
Tingting Wang
Lingkai Su
Ying Wang
Yadong Chen
Jie Zhang
Yun Huang
Suman Tong
Cheng Zhou
Shuli Deng
Nan Qin
spellingShingle Yuan Wang
Sa Wang
Chunyan Wu
Xi Chen
Zhuhui Duan
Qian Xu
Wen Jiang
Lei Xu
Tingting Wang
Lingkai Su
Ying Wang
Yadong Chen
Jie Zhang
Yun Huang
Suman Tong
Cheng Zhou
Shuli Deng
Nan Qin
Oral Microbiome Alterations Associated with Early Childhood Caries Highlight the Importance of Carbohydrate Metabolic Activities
mSystems
early childhood caries
metagenomics
oral microbiome
functional profile
preschool children
author_facet Yuan Wang
Sa Wang
Chunyan Wu
Xi Chen
Zhuhui Duan
Qian Xu
Wen Jiang
Lei Xu
Tingting Wang
Lingkai Su
Ying Wang
Yadong Chen
Jie Zhang
Yun Huang
Suman Tong
Cheng Zhou
Shuli Deng
Nan Qin
author_sort Yuan Wang
title Oral Microbiome Alterations Associated with Early Childhood Caries Highlight the Importance of Carbohydrate Metabolic Activities
title_short Oral Microbiome Alterations Associated with Early Childhood Caries Highlight the Importance of Carbohydrate Metabolic Activities
title_full Oral Microbiome Alterations Associated with Early Childhood Caries Highlight the Importance of Carbohydrate Metabolic Activities
title_fullStr Oral Microbiome Alterations Associated with Early Childhood Caries Highlight the Importance of Carbohydrate Metabolic Activities
title_full_unstemmed Oral Microbiome Alterations Associated with Early Childhood Caries Highlight the Importance of Carbohydrate Metabolic Activities
title_sort oral microbiome alterations associated with early childhood caries highlight the importance of carbohydrate metabolic activities
publisher American Society for Microbiology
series mSystems
issn 2379-5077
publishDate 2019-11-01
description Dental caries is a highly prevalent oral disease that can lead to severe dental damage and may greatly compromise the quality of life of the affected individuals. Previous studies, including those based on 16S rRNA gene, have revealed that the oral microbiota plays a prominent role in development of the disease. But the approach of those studies was limited in analyzing several key microbiome traits, including species- or strain-level composition and functional profile. Here, we performed metagenomic analyses for a cohort of preschool children with or without caries. Our results showed that caries was associated with extensive microbiota differences at various taxonomic and functional levels. Some caries-associated species had not been previously reported, some of which may have significant clinical implications. A microbiome gene catalogue from children with caries was constructed for the first time. The results demonstrated that caries is associated with alterations of the oral microbiome, including changes in microbial composition and metabolic functional profile.Globally, dental caries is the most prevalent chronic oral disease and affects roughly half of all children. The aim of this report was to use metagenomic analyses to investigate the relationship between the oral microbiome and caries in preschool children. A total of 25 preschoolers, aged 3 to 5 years old with severe early childhood caries (ECC), and 19 age-matched, caries-free children as controls were recruited. Saliva samples were collected from the participants and were subjected to metagenomic analyses, whereby the oral microbial communities were investigated. The metagenomic analyses revealed substantial microbiota differences between the two groups, indicating apparent shifts of the oral microbiome present in the ECC group. At the species level, the ECC-enriched microbes included Prevotella amnii, Shuttleworthia satelles, Olsenella uli, and Anaeroglobus geminatus. Interestingly, Actinomyces odontolyticus and Actinomyces graevenitzii exhibited apparent differences at the strain level but not the species level between the ECC and control groups. Functional examination showed that the ECC group displayed extensive alterations in metabolic genes/pathways/modules, including enriched functions in sugar metabolism. Finally, an SVM (support vector machine) classifier comprising seven species was developed and generated a moderately good performance in predicting caries onset (area under the receiver operating characteristic curve [AUC] = 78.33%). Together, these findings indicate that caries is associated with considerable changes in the oral microbiome, some of which can potentially be exploited as therapeutic targets or diagnostic markers. (This study has been registered at ClinicalTrials.gov under registration no. NCT02341352.)
topic early childhood caries
metagenomics
oral microbiome
functional profile
preschool children
url https://doi.org/10.1128/mSystems.00450-19
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