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Deep metagenomics examines the oral microbiome during dental caries, revealing novel taxa and co-occurrences with host molecules.

ABSTRACT: Dental caries, the most common chronic infectious disease worldwide, has a complex etiology involving the interplay of microbial and host factors that are not completely understood. In this study, the oral microbiome and 38 host cytokines and chemokines were analyzed across 23 children with caries and 24 children with healthy dentition. De novo assembly of metagenomic sequencing obtained 527 metagenome-assembled genomes (MAGs), representing 150 bacterial species. Forty-two of these species had no genomes in public repositories, thereby representing novel taxa. These new genomes greatly expanded the known pangenomes of many oral clades, including the enigmatic Saccharibacteria clades G3 and G6, which had distinct functional repertoires compared to other oral Saccharibacteria. Saccharibacteria are understood to be obligate epibionts, which are dependent on host bacteria. These data suggest that the various Saccharibacteria clades may rely on their hosts for highly distinct metabolic requirements, which would have significant evolutionary and ecological implications. Across the study group, Rothia, Neisseria, and Haemophilus spp. were associated with good dental health, whereas Prevotella spp., Streptococcus mutans, and Human herpesvirus 4 (Epstein-Barr virus [EBV]) were more prevalent in children with caries. Finally, 10 of the host immunological markers were significantly elevated in the caries group, and co-occurrence analysis provided an atlas of potential relationships between microbes and host immunological molecules. Overall, this study illustrated the oral microbiome at an unprecedented resolution and contributed several leads for further study that will increase the understanding of caries pathogenesis and guide therapeutic development.

SUBMITTER: Baker JL

PROVIDER: S-EPMC7849383 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Deep metagenomics examines the oral microbiome during dental caries, revealing novel taxa and co-occurrences with host molecules.

Baker Jonathon L JL Morton James T JT Dinis Márcia M Alvarez Ruth R Tran Nini C NC Knight Rob R Edlund Anna A

Genome research 20201125 1

Dental caries, the most common chronic infectious disease worldwide, has a complex etiology involving the interplay of microbial and host factors that are not completely understood. In this study, the oral microbiome and 38 host cytokines and chemokines were analyzed across 23 children with caries and 24 children with healthy dentition. De novo assembly of metagenomic sequencing obtained 527 metagenome-assembled genomes (MAGs), representing 150 bacterial species. Forty-two of these species had n ...[more]

PMID: 33239396

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Project description:With the aging of the population, dental caries in the elderly has received increasing attention. A comprehensive study of the oral microbiome is required to understand its polymicrobial etiology. The results of previous studies are limited and remain controversial. In this study, subjects 60 years and older with and without caries were recruited. Unstimulated saliva and dental plaque were collected from each subject and the bacterial 16S rDNA was amplified using PCR and sequenced by Illumina MiSeq high-throughput sequencing. A total of 92 samples were collected from 24 caries patients and 22 healthy controls. Sequences clustered into 147,531 OTUs, representing 16 phyla, 29 classes, 49 orders, 79 families, 149 genera, and 305 species. All predominant phyla, including Proteobacteria, Bacteroidetes, Firmicutes, Fusobacteria, Actinobacteria, and Saccharibacteria, were largely consistent in different groups, but different relative abundances could be observed. The core microbiome was defined with 246 shared species among groups, which occupied 80.7% of all the species detected. Alpha diversity showed no significant differences in bacterial richness or diversity between caries patients and healthy controls, but distinction existed between samples collected from dental plaque and saliva. Beta diversity analysis was performed by PCoA and hierarchical clustering analysis, showing similar results that microorganisms vary between the two niches. The biomarkers of different groups were defined by LEfSe analysis to identify potential caries-related and health-related bacteria. The co-occurrence analysis of the predominant genera revealed significant interactions among oral microbiota and exhibited more complex and aggregated bacterial correlations in caries-free groups. Finally, the functional prediction of the microbiota present in oral samples was performed by PICRUSt, indicating vigorous microbial metabolism in the oral bacterial community. Our study provides thorough knowledge of the microbiological etiology of elderly individuals with caries and is expected to provide novel methods for its prevention and treatment.

Project description:Oral diseases, such as periodontal disease and dental caries, have a high risk of recurrence and are considered to be related to dysbiosis of the oral microbiome and metabolome. It is, therefore, important to understand the state of the oral microbiome and metabolome after disease treatment to prevent recurrence. The current study sought to clarify whether oral dysbiosis improves the following remission of symptoms by dental treatment. To this end, the salivary microbiome and metabolome of healthy participants were compared to those with periodontal disease, dental caries, or both (concurrent). Saliva was collected as mouth-rinsed water and the microbiome was measured using 16S rRNA gene targeted sequencing and metabolome using capillary electrophoresis-time-of-flight mass spectrometry. Comparisons with healthy participants were performed before and after treatment, and several months after transition to self-care. Dental treatment significantly improved the oral health condition of each group; several months after treatment, oral health did not deteriorate. However, even after remission, the salivary microbiome of the two groups (oral disease and healthy) differed significantly. Additionally, after remission, significant differences, compared with healthy participants, remained in the relative abundances of disease-related bacteria and nitrate-reducing bacteria. After remission, significant differences were observed in the salivary metabolome in the healthy group in terms of threonate and pyrimidine metabolism-related component concentrations, which are assumed to reflect the high relative abundance of periodontal disease-related bacteria in the microbiome. Oral microbiome dysbiosis persisted even after dental treatment-induced disease remission with a sustained increased risk of disease when compared with healthy participants. IMPORTANCE We characterized the oral conditions, salivary microbiome, and metabolome after dental treatment by investigating the state after treatment completion and transition to self-care. Dental treatment improved oral health conditions, resulting in oral disease remission; however, the imbalanced state of the salivary microbiome continued even after remission. Although the results of this study are preliminary, owing to the small number of participants in each group when compared to larger cohort studies, they indicate that the risk of disease may remain higher than that of healthy participants, thereby demonstrating the importance of removing dental plaque containing disease-related bacteria using appropriate care even after treatment completion. We also identified bacterial species with relative abundances that differed from those of healthy participants even after remission of symptoms, which may indicate that the maturation of certain bacterial species must be controlled to improve the oral microbiome and reduce the risk of disease recurrence.

Project description:IntroductionA lower prevalence of dental caries (hereafter termed "caries") has been observed in children with dental extrinsic black stain (EBS).MethodsWe investigated the epidemiologic characterization of EBS and explored the possible role of the oral microbiome (OM) and gut microbiome (GM) in EBS formation and caries prevention. In an epidemiologic survey, 2,675 children aged 3-6 years were included. Thirty-eight of these children (7 children had both caries and EBS, 10 had EBS only, 11 had caries only, and 10 were healthy children) were recruited for 16S rRNA sequencing and collection of samples of supragingival plaque and feces. Collected plaque samples were divided into four groups: BCP (EBS+, caries+), BP (EBS+, caries-), CP (EBS-, caries+), and P (EBS-, caries-). Fecal samples were also divided into four groups: BCF (EBS+, caries+), BF (EBS+, caries-), CF (EBS-, caries+), and F (EBS-, caries-).ResultsEBS was observed in 12.10% of this population. Children with EBS had a significantly reduced prevalence of caries and a lower mean value of decayed-missing-filled teeth (dmft; p < 0.01). According to analyses of dental plaque, the P group had the most complex microbiome. The BCP group exhibited greater operational taxonomic unit (OTU) richness but a reduced evenness compared with the BP group, and the CP group showed greater OTU richness than the BP group. At the genus level, higher abundance of Actinomyces and Cardiobacterium species was observed in the BCP group. Higher abundance of Lautropia and Pesudopropionibacteriumin species was observed in the BP group compared with P and CP groups, respectively (p < 0.05). Veillonella species were significantly more common in P and CP groups than in BP groups, whereas Porphyromonas and Fusobacterium species were more common in the CP group (p < 0.05). With regard to the GM, the CF group exhibited greater OTU diversity than the BF group. The GM in the BCF group exhibited the most complex relationships across all fecal groups. GM groups could be distinguished by various unique biomarkers, such as Escherichia and Shigella species in the BCF group, Agathobacter and Ruminococcus species in the CF group, Lactobacillus species in the BF group, and Roseburia species in the F group. Our results suggest that EBS is a possible protective factor against early-childhood caries. Dental plaque and the GM may be relevant to EBS in primary dentition.

Project description:BackgroundSuboptimal maternal oral health during pregnancy is potentially associated with adverse birth outcomes and increased dental caries risks in children. This study aimed to assess the oral microbiome and immune response following an innovative clinical regimen, Prenatal Total Oral Rehabilitation (PTOR), that fully restores women's oral health to a "disease-free status" before delivery.MethodsThis prospective cohort study assessed 15 pregnant women at baseline and 3 follow-up visits (1 week, 2 weeks, and 2 months) after receiving PTOR. The salivary and supragingival plaque microbiomes were analyzed using metagenomic sequencing. Multiplexed Luminex cytokine assays were performed to examine immune response following PTOR. The association between salivary immune markers and oral microbiome was further examined.ResultsPTOR was associated with a reduction of periodontal pathogens in plaque, for instance, a lower relative abundance of Tannerella forsythia and Treponema denticola at 2 weeks compared to the baseline (p < 0.05). The alpha diversity of plaque microbial community was significantly reduced at the 1-week follow-up (p < 0.05). Furthermore, we observed significant changes in the Actinomyces defective-associated carbohydrate degradation pathway and Streptococcus Gordonii-associated fatty acid biosynthesis pathway. Two immune markers related to adverse birth outcomes significantly differed between baseline and follow-up. ITAC, negatively correlated with preeclampsia severity, significantly increased at 1-week follow-up; MCP-1, positively correlated with gestational age, was elevated at 1-week follow-up. Association modeling between immune markers and microbiome further revealed specific oral microorganisms that are potentially correlated with the host immune response.ConclusionsPTOR is associated with alteration of the oral microbiome and immune response among a cohort of underserved US pregnant women. Future randomized clinical trials are warranted to comprehensively assess the impact of PTOR on maternal oral flora, birth outcomes, and their offspring's oral health.

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Deep metagenomics examines the oral microbiome during dental caries, revealing novel taxa and co-occurrences with host molecules.

Publications

Deep metagenomics examines the oral microbiome during dental caries, revealing novel taxa and co-occurrences with host molecules.

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