Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome

AbstractMicrobial residents of the human oral cavity have long been a major focus of microbiology due to their influence on host health and their intriguing patterns of site specificity amidst the lack of dispersal limitation. Yet, the determinants of niche partitioning in this habitat are yet to be fully understood, especially among the taxa that belong to recently discovered branches of microbial life. Here we assembled metagenomes from daily tongue and dental plaque samples from multiple individuals and reconstructed 790 non-redundant genomes, 43 of which resolved to TM7 that formed six monophyletic clades distinctly associated either with plaque or with tongue. Both pangenomic and phylogenomic analyses grouped tongue-specific TM7 clades with other host-associated TM7 genomes. In contrast, plaque-specific TM7 grouped together with environmental TM7 genomes. Besides offering deeper insights into the ecology, evolution, and the mobilome of the cryptic members of the oral microbiome, our study reveals an intriguing resemblance between dental plaque and non-host environments indicated by the TM7 evolution, suggesting that plaque may have served as a stepping stone for environmental microbes to adapt to host environments for some clades of human associated microbes. Additionally, we report that prophages are widespread amongst oral-associated TM7, while absent from environmental TM7, suggesting that prophages may have played a role in adaptation of TM7 to the host environment.

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Functional and genetic markers of niche partitioning among enigmatic members of the human oral microbiome

Genome Biology ◽

10.1186/s13059-020-02195-w ◽

2020 ◽

Vol 21 (1) ◽

Author(s):

Alon Shaiber ◽

Amy D. Willis ◽

Tom O. Delmont ◽

Simon Roux ◽

Lin-Xing Chen ◽

...

Keyword(s):

Oral Cavity ◽

Dental Plaque ◽

Niche Partitioning ◽

Dispersal Limitation ◽

Oral Microbiome ◽

Microbial Life ◽

Host Health ◽

Phylogenomic Analyses ◽

Candidate Phyla Radiation ◽

Environmental Microbes

Abstract Introduction Microbial residents of the human oral cavity have long been a major focus of microbiology due to their influence on host health and intriguing patterns of site specificity amidst the lack of dispersal limitation. However, the determinants of niche partitioning in this habitat are yet to be fully understood, especially among taxa that belong to recently discovered branches of microbial life. Results Here, we assemble metagenomes from tongue and dental plaque samples from multiple individuals and reconstruct 790 non-redundant genomes, 43 of which resolve to TM7, a member of the Candidate Phyla Radiation, forming six monophyletic clades that distinctly associate with either plaque or tongue. Both pangenomic and phylogenomic analyses group tongue-specific clades with other host-associated TM7 genomes. In contrast, plaque-specific TM7 group with environmental TM7 genomes. Besides offering deeper insights into the ecology, evolution, and mobilome of cryptic members of the oral microbiome, our study reveals an intriguing resemblance between dental plaque and non-host environments indicated by the TM7 evolution, suggesting that plaque may have served as a stepping stone for environmental microbes to adapt to host environments for some clades of microbes. Additionally, we report that prophages are widespread among oral-associated TM7, while absent from environmental TM7, suggesting that prophages may have played a role in adaptation of TM7 to the host environment. Conclusions Our data illuminate niche partitioning of enigmatic members of the oral cavity, including TM7, SR1, and GN02, and provide genomes for poorly characterized yet prevalent members of this biome, such as uncultivated Flavobacteriaceae.

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The dental calculus metabolome in modern and historic samples

10.1101/136176 ◽

2017 ◽

Cited By ~ 1

Author(s):

Irina M. Velsko ◽

Katherine A. Overmyer ◽

Camilla Speller ◽

Matthew Collins ◽

Louise Loe ◽

...

Keyword(s):

Dental Plaque ◽

Ultra Performance Liquid Chromatography ◽

Oral Microbiome ◽

Chemical Degradation ◽

Dental Calculus ◽

Metabolite Profiles ◽

Free Nucleotides ◽

Liquid Chromatography Tandem Mass ◽

Long Time

AbstractIntroductionDental calculus is a mineralized microbial dental plaque biofilm that forms throughout life by precipitation of salivary calcium salts. Successive cycles of dental plaque growth and calcification make it an unusually well-preserved, long-term record of host-microbial interaction in the archaeological record. Recent studies have confirmed the survival of authentic ancient DNA and proteins within historic and prehistoric dental calculus, making it a promising substrate for investigating oral microbiome evolution via direct measurement and comparison of modern and ancient specimens.ObjectiveWe present the first comprehensive characterization of the human dental calculus metabolome using a multi-platform approach.MethodsUltra performance liquid chromatography-tandem mass spectrometry (UPLC-MS/MS) quantified 285 metabolites in modern and historic (200 years old) dental calculus, including metabolites of drug and dietary origin. A subset of historic samples was additionally analyzed by high-resolution gas chromatography-MS (GC-MS) and UPLC- MS/MS for further characterization of polar metabolites and lipids, respectively. Metabolite profiles of modern and historic calculus were compared to identify patterns of persistence and loss.ResultsDipeptides, free amino acids, free nucleotides, and carbohydrates substantially decrease in abundance and ubiquity in archaeological samples, with some exceptions. Lipids generally persist, and saturated and mono-unsaturated medium and long chain fatty acids appear to be well-preserved, while metabolic derivatives related to oxidation and chemical degradation are found at higher levels in archaeological dental calculus than fresh samples.ConclusionsThe results of this study indicate that certain metabolite classes have higher potential for recovery over long time scales and may serve as appropriate targets for oral microbiome evolutionary studies.

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Antimicrobial and Substantivity Properties of Silver Nanoparticles against Oral Microbiomes Clinically Isolated from Young and Young-Adult Patients

Journal of Nanomaterials ◽

10.1155/2019/3205971 ◽

2019 ◽

Vol 2019 ◽

pp. 1-14 ◽

Cited By ~ 2

Author(s):

León Francisco Espinosa-Cristóbal ◽

Carolina Holguín-Meráz ◽

Erasto Armando Zaragoza-Contreras ◽

Rita Elizabeth Martínez-Martínez ◽

Alejandro Donohue-Cornejo ◽

...

Keyword(s):

Silver Nanoparticles ◽

Young Adult ◽

Dental Caries ◽

Periodontal Disease ◽

Dental Plaque ◽

Bacterial Species ◽

Inhibitory Effect ◽

Oral Bacteria ◽

Oral Microbiome ◽

Oral Biofilms

The dental plaque is an oral microbiome hardly associated to be the etiological agent of dental caries and periodontal disease which are still considered serious health public problems. Silver nanoparticles (AgNPs) have demonstrated to have good antimicrobial properties affecting a wide variety of microorganisms, including oral bacteria; however, there is no scientific information that has evaluated the antimicrobial effect of AgNPs against clinical oral biofilms associated with dental caries and periodontal disease. The aim of this study was to determine the antimicrobial and substantivity effects of AgNPs in oral biofilms isolated clinically from patients with dental caries and periodontal disease. Sixty-seven young and young-adult subjects with dental caries and periodontal disease were clinically sampled through the collection of subgingival dental plaque. The inhibitory effect of AgNPs was performed with standard microbiological assays by triplicate using two sizes of particle. Polymerase chain reaction (PCR) assay was used to identify the presence of specific bacterial species. All AgNPs showed an inhibitory effect for all oral biofilms for any age and, generally, any gender (p>0.05); however, the effectiveness of the antimicrobial and substantivity effects was related to particle size, time, and gender (p<0.05). The identified microorganisms were S. mutans, S. sobrinus, S. sanguinis, S. gordonii, S. oralis, P. gingivalis, T. forsythia, and P. intermedia. The AgNPs could be considered as a potential antimicrobial agent for the control and prevention of dental caries and periodontal disease.

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Site-specificity of streptococci in the oral microbiome

10.1101/2021.11.29.470446 ◽

2021 ◽

Author(s):

Anthony R. McLean ◽

Julian Torres-Morales ◽

Gary G. Borisy ◽

Jessica L. Mark Welch

Keyword(s):

Oral Cavity ◽

Related Species ◽

Oral Microbiome ◽

Individual Species ◽

Rrna Gene ◽

Site Specificity ◽

Oral Streptococci ◽

Closely Related Species ◽

Streptococcus Species ◽

Human Oral Cavity

Patterns of microbial distribution are determined by as-yet poorly understood rules governing where microbes can grow and thrive. Therefore, a detailed understanding of where bacteria localize is necessary to advance microbial ecology and microbiome-based therapeutics. The site-specialist hypothesis predicts that most microbes in the human oral cavity have a primary habitat within the mouth where they are most abundant. We asked whether this hypothesis accurately describes the distribution of the members of the genus Streptococcus, a clinically relevant taxon that dominates most oral sites. Prior analysis of 16S rRNA gene sequencing data indicated that some oral Streptococcus clades are site-specialists while others may be generalists. However, within complex microbial populations composed of numerous closely-related species and strains, such as the oral streptococci, genome-scale analysis is necessary to provide the resolution to discriminate closely related taxa with distinct functional roles. Here we assess whether individual species within this genus are generalists using publicly available genomic sequence data that provides species-level resolution. We chose a set of high-quality representative genomes for Streptococcus species from the human oral microbiome. Onto these genomes, we mapped short-read metagenomic sequences from supragingival plaque, tongue dorsum, and other sites in the oral cavity. We found that every reliably detectable Streptococcus species in the human oral cavity was a site-specialist and that even closely related species such as S. mitis, S. oralis, and S. infantis specialized in different sites. These findings indicate that closely related bacteria can have distinct habitat distributions in the absence of dispersal limitation and under similar environmental conditions and immune regimes. These three species also share substantially the same species-specific core genes indicating that neither taxonomy nor gene content are clear predictors of site-specialization. Site-specificity may instead be influenced by subtle characteristics such as nucleotide-level divergences within conserved genes.

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Functional Profiling of Saliva Microbiome is Essential for Oral Cancer Prediction

10.21203/rs.3.rs-45330/v1 ◽

2020 ◽

Author(s):

Jiung-Wen Chen ◽

Wei-Fan Chiang ◽

Jer-Horng Wu ◽

Yuh-Ling Chen ◽

Wei-Sheng Wu ◽

...

Keyword(s):

Machine Learning ◽

Oral Cancer ◽

Bacterial Communities ◽

Predictive Performance ◽

Oral Microbiome ◽

Oral Carcinogenesis ◽

Verrucous Hyperplasia ◽

Host Health ◽

Functional Profiling ◽

And Function

Abstract Background: The association between microbiome and host disease has been documented in oral cancer, one of the leading cancers worldwide. Huge efforts are made to use the profile of oral microbiome and distinct signature species as markers to distinguish oral cancer patients from healthy individuals. The previous results, however, remain inconclusive. The assembly mechanisms of oral microbiome and their response to changes in oral carcinogenesis also have not been characterized. Here, using 16S rRNA gene amplicon sequencing and in-silico function prediction approaches, we analyzed the saliva microbiome in cohorts of orally healthy, oral verrucous hyperplasia, and oral cancer at taxon and function levels, and compared their corresponding predictive performance of oral cancer using machine learning algorithms.Results: Analyses of diversity and phylogenetic profiles of bacterial communities in saliva showed that microbiome dysbiosis was significantly linked to oral health status. As oral health deteriorated, the number of core species (>75% prevalence) as a percentage of overall species richness declined. In line with the null model-based analysis, taxonomic and functional assemblies of saliva microbiomes were primarily governed by the stochastic processes. Correspondingly, the quantitative assessment of partitioned beta-diversity suggested extremely high species turnover but low function turnover, revealing a functional redundancy of the oral ecosystem. Functional beta-diversity in salvia microbiome shifted from turnover to nestedness during carcinogenesis of oral verrucous hyperplasia, but this pattern was not observed at the taxon level. Moreover, using both taxon and function data as training features for machine learning-aided prediction on host health status supports a superior predictive performance when using functional profiling. Similar results were also obtained and validated using publicly accessible data.Conclusions: Our results suggest that altered oral bacterial communities are highly associated with carcinogenesis of oral verrucous hyperplasia. Partly owing to high taxonomic turnover and stochastic assembly processes of the oral ecosystem, discovering oral microbial consortia as universal biomarkers for oral cancer may prove difficult and arduous. Functional profiles are relatively stable and evolve a nestedness pattern during oral carcinogenesis, serving as a new benchmark to study the interplay of the oral microbiome and host health in the future.

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Substantial Differences in the Subgingival Microbiome Measured by 16S Metagenomics According to Periodontitis Status in Older Women

Dentistry Journal ◽

10.3390/dj6040058 ◽

2018 ◽

Vol 6 (4) ◽

pp. 58 ◽

Cited By ~ 5

Author(s):

Michael LaMonte ◽

Robert Genco ◽

Wei Zheng ◽

Daniel McSkimming ◽

Christopher Andrews ◽

...

Keyword(s):

Postmenopausal Women ◽

Krebs Cycle ◽

Later Life ◽

Oral Microbiome ◽

Host Susceptibility ◽

Rrna Gene ◽

Periodontal Pathogens ◽

Microbial Life ◽

Severe Periodontitis ◽

V3 Region

Aging invokes physiological changes, such as immunosenescence and inflammation, that could increase host susceptibility to oral microbiome shifts that enable periodontitis progression in later life. At present, there is a dearth of studies specifically evaluating the oral microbiome and periodontitis in older adults. We used high-throughput untargeted sequencing methods and functional metagenomic analyses to assess and compare the subgingival biofilm of postmenopausal women (mean age 71 years) according to periodontitis status. Subgingival plaque samples were obtained from 15 postmenopausal women with no periodontitis, and from 15 women with severe periodontitis, determined by probing measures. The 16S rRNA gene (V1–V3 region) was sequenced on the 454 FLX platform. The PICRUSt technique was used to provide information on what the potential functional characteristics of microbiota might be in healthy, compared with diseased, periodontium. The subgingival microbiome associated with periodontitis showed clear differences to that associated with health. Of the 464 species identified, 22.8% had elevated abundance in disease, while only 6.3% had elevated abundance in health. Among the 12 most prevalent organisms in periodontitis, one-half have previously been recognized as periodontal pathogens by other investigators. The subgingival microbiome in periodontitis contained genes that could code for specific activities, including microbial mobility, synthesis of endotoxin, and proteolytic degradation. The healthy microbiome included genes that could code for sustaining microbial life, including encoding for transporters, glycolysis, gluconeogenesis, the Krebs cycle, and protein kinases. In the present study on postmenopausal women, aged 60 and older, the subgingival microbiome differed in composition and potential function between those with and without periodontitis. Studies of functional gene expression, such as transcriptomics, are needed to definitively identify the molecules carrying out functions associated with pathogenic subgingival complexes. This, in turn, could lead to identification of targets for enhanced management of periodontitis and, possibly, other diseases, in later life.

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Altered Oral Viral Ecology in Association with Periodontal Disease

mBio ◽

10.1128/mbio.01133-14 ◽

2014 ◽

Vol 5 (3) ◽

Cited By ~ 68

Author(s):

Melissa Ly ◽

Shira R. Abeles ◽

Tobias K. Boehm ◽

Refugio Robles-Sikisaka ◽

Mayuri Naidu ◽

...

Keyword(s):

Health Status ◽

Oral Health ◽

Periodontal Disease ◽

Bacterial Communities ◽

Dental Plaque ◽

Oral Health Status ◽

Oral Microbiome ◽

Oral Biofilm ◽

Viral Communities ◽

Health And Disease

ABSTRACTThe human oral cavity is home to a large and diverse community of viruses that have yet to be characterized in patients with periodontal disease. We recruited and sampled saliva and oral biofilm from a cohort of humans either periodontally healthy or with mild or significant periodontal disease to discern whether there are differences in viral communities that reflect their oral health status. We found communities of viruses inhabiting saliva and the subgingival and supragingival biofilms of each subject that were composed largely of bacteriophage. While there were homologous viruses common to different subjects and biogeographic sites, for most of the subjects, virome compositions were significantly associated with the oral sites from which they were derived. The largest distinctions between virome compositions were found when comparing the subgingival and supragingival biofilms to those of planktonic saliva. Differences in virome composition were significantly associated with oral health status for both subgingival and supragingival biofilm viruses but not for salivary viruses. Among the differences identified in virome compositions was a significant expansion of myoviruses in subgingival biofilm, suggesting that periodontal disease favors lytic phage. We also characterized the bacterial communities in each subject at each biogeographic site by using the V3 hypervariable segment of the 16S rRNA and did not identify distinctions between oral health and disease similar to those found in viral communities. The significantly altered ecology of viruses of oral biofilm in subjects with periodontal disease compared to that of relatively periodontally healthy ones suggests that viruses may serve as useful indicators of oral health status.IMPORTANCELittle is known about the role or the constituents of viruses as members of the human microbiome. We investigated the composition of human oral viral communities in a group of relatively periodontally healthy subjects or significant periodontitis to determine whether health status may be associated with differences in viruses. We found that most of the viruses present were predators of bacteria. The viruses inhabiting dental plaque were significantly different on the basis of oral health status, while those present in saliva were not. Dental plaque viruses in periodontitis were predicted to be significantly more likely to kill their bacterial hosts than those found in healthy mouths. Because oral diseases such as periodontitis have been shown to have altered bacterial communities, we believe that viruses and their role as drivers of ecosystem diversity are important contributors to the human oral microbiome in health and disease states.

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The Postmedieval Latvian Oral Microbiome in the Context of Modern Dental Calculus and Modern Dental Plaque Microbial Profiles

Genes ◽

10.3390/genes12020309 ◽

2021 ◽

Vol 12 (2) ◽

pp. 309

Author(s):

Alisa Kazarina ◽

Elina Petersone-Gordina ◽

Janis Kimsis ◽

Jevgenija Kuzmicka ◽

Pawel Zayakin ◽

...

Keyword(s):

Dental Plaque ◽

Modern Human ◽

Oral Microbiome ◽

Dental Calculus ◽

Microbial Composition ◽

Metagenome Analysis ◽

Microbiome Composition ◽

Microbial Adaptation ◽

Microbial Dna ◽

Insight Into

Recent advantages in paleomicrobiology have provided an opportunity to investigate the composition of ancient microbial ecologies. Here, using metagenome analysis, we investigated the microbial profiles of historic dental calculus retrieved from archaeological human remains from postmedieval Latvia dated 16–17th century AD and examined the associations of oral taxa and microbial diversity with specific characteristics. We evaluated the preservation of human oral microbiome patterns in historic samples and compared the microbial composition of historic dental calculus, modern human dental plaque, modern human dental calculus samples and burial soil microbiota. Overall, the results showed that the majority of microbial DNA in historic dental calculus originated from the oral microbiome with little impact of the burial environment. Good preservation of ancient DNA in historical dental calculus samples has provided reliable insight into the composition of the oral microbiome of postmedieval Latvian individuals. The relative stability of the classifiable oral microbiome composition was observed. Significant differences between the microbiome profiles of dental calculus and dental plaque samples were identified, suggesting microbial adaptation to a specific human body environment.

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Comparison of Periodontal Bacteria of Edo and Modern Periods Using Novel Diagnostic Approach for Periodontitis With Micro-CT

Frontiers in Cellular and Infection Microbiology ◽

10.3389/fcimb.2021.723821 ◽

2021 ◽

Vol 11 ◽

Author(s):

Takahiko Shiba ◽

Keiji Komatsu ◽

Takeaki Sudo ◽

Rikai Sawafuji ◽

Aiko Saso ◽

...

Keyword(s):

16S Rdna ◽

Dental Plaque ◽

Pathogenic Bacteria ◽

Oral Microbiome ◽

Diagnostic Approach ◽

Dental Calculus ◽

Micro Computed Tomography ◽

Modern Humans ◽

Bacterial Composition ◽

The Core

Ancient dental calculus, formed from dental plaque, is a rich source of ancient DNA and can provide information regarding the food and oral microbiology at that time. Genomic analysis of dental calculus from Neanderthals has revealed the difference in bacterial composition of oral microbiome between Neanderthals and modern humans. There are few reports investigating whether the pathogenic bacteria of periodontitis, a polymicrobial disease induced in response to the accumulation of dental plaque, were different between ancient and modern humans. This study aimed to compare the bacterial composition of the oral microbiome in ancient and modern human samples and to investigate whether lifestyle differences depending on the era have altered the bacterial composition of the oral microbiome and the causative bacteria of periodontitis. Additionally, we introduce a novel diagnostic approach for periodontitis in ancient skeletons using micro-computed tomography. Ancient 16S rDNA sequences were obtained from 12 samples at the Unko-in site (18th-19th century) of the Edo era (1603–1867), a characteristic period in Japan when immigrants were not accepted. Furthermore, modern 16S rDNA data from 53 samples were obtained from a database to compare the modern and ancient microbiome. The microbial co-occurrence network was analyzed based on 16S rDNA read abundance. Eubacterium species, Mollicutes species, and Treponema socranskii were the core species in the Edo co-occurrence network. The co-occurrence relationship between Actinomyces oricola and Eggerthella lenta appeared to have played a key role in causing periodontitis in the Edo era. However, Porphyromonas gingivalis, Fusobacterium nucleatum subsp. vincentii, and Prevotella pleuritidis were the core and highly abundant species in the co-occurrence network of modern samples. These results suggest the possibility of differences in the pathogens causing periodontitis during different eras in history.

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Characterization of Supragingival Plaque and Oral Swab Microbiomes in Children With Severe Early Childhood Caries

Frontiers in Microbiology ◽

10.3389/fmicb.2021.683685 ◽

2021 ◽

Vol 12 ◽

Author(s):

Vivianne Cruz de Jesus ◽

Mohd Wasif Khan ◽

Betty-Anne Mittermuller ◽

Kangmin Duan ◽

Pingzhao Hu ◽

...

Keyword(s):

Early Childhood ◽

Dental Plaque ◽

Early Childhood Caries ◽

Oral Microbiome ◽

Rrna Genes ◽

Oral Swab ◽

Supragingival Plaque ◽

Severe Early Childhood Caries ◽

Childhood Caries

The human oral cavity harbors one of the most diverse microbial communities with different oral microenvironments allowing the colonization of unique microbial species. This study aimed to determine which of two commonly used sampling sites (dental plaque vs. oral swab) would provide a better prediction model for caries-free vs. severe early childhood caries (S-ECC) using next generation sequencing and machine learning (ML). In this cross-sectional study, a total of 80 children (40 S-ECC and 40 caries-free) < 72 months of age were recruited. Supragingival plaque and oral swab samples were used for the amplicon sequencing of the V4-16S rRNA and ITS1 rRNA genes. The results showed significant differences in alpha and beta diversity between dental plaque and oral swab bacterial and fungal microbiomes. Differential abundance analyses showed that, among others, the cariogenic species Streptococcus mutans was enriched in the dental plaque, compared to oral swabs, of children with S-ECC. The fungal species Candida dubliniensis and C. tropicalis were more abundant in the oral swab samples of children with S-ECC compared to caries-free controls. They were also among the top 20 most important features for the classification of S-ECC vs. caries-free in oral swabs and for the classification of dental plaque vs. oral swab in the S-ECC group. ML approaches revealed the possibility of classifying samples according to both caries status and sampling sites. The tested site of sample collection did not change the predictability of the disease. However, the species considered to be important for the classification of disease in each sampling site were slightly different. Being able to determine the origin of the samples could be very useful during the design of oral microbiome studies. This study provides important insights into the differences between the dental plaque and oral swab bacteriome and mycobiome of children with S-ECC and those caries-free.

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