Supragingival plaque microbiome ecology and functional potential in the context of health and disease

Espinoza, Josh L.; Harkins, Derek M.; Torralba, Manolito; Gómez, Andrés; Highlander, Sarah K.; Jones, Marcus B.; Leong, Pamela; Saffery, Richard; Bockmann, Michelle; Kuelbs, Claire; Inman, Jason M.; Hughes, Toby; Craig, Jeffrey M.; Nelson, Karen E.; Dupont, Chris L.

doi:10.1101/325407

Cited by 5 publications

(12 citation statements)

References 71 publications

(101 reference statements)

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“…This indicates that S. mutans, when present, has a large influence on the pathogenicity of the oral microbiome due to its prodigious capacity to generate insoluble glucans and resultant biofilms (9, 26). Other oral microbiome studies have found S. mutans at low abundances (20, 21, 54), and the use of saliva in this study may explain its rarity, and possibly underestimation, here—as an exceptional biofilm-former, it is less likely to be shed from its dental plaque residence into the salivary milieu (55).…”

Section: Discussionmentioning

confidence: 60%

“…S. gordonii ), further illustrating a need for studies utilizing more in-depth sequencing and analysis methods (5). Although several shotgun metagenomic surveys of the oral microbiota have been performed (20–23), they have not employed differential ranking techniques with consistent reference frames, as detailed in Morton et al 2019 (13).…”

Section: Introductionmentioning

confidence: 99%

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

Baker

Morton

Dinis³

et al. 2019

Preprint

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45Dental caries is the most common chronic infectious disease globally. The microbial communities 46 associated with caries have mainly been examined using relatively low-resolution 16S rRNA gene 47 amplicon sequencing and/or using downstream analyses that are unsound for the compositional 48 nature of the data provided by sequencing. Additionally, the relationship between caries, oral 49 microbiome composition, and host immunological markers has not been explored. In this study, 50 the oral microbiome and a panel of 38 host markers was analyzed across the saliva from 23 51 children with dentin caries and 24 children with healthy dentition. Metagenomic sequencing, 52 followed by investigation using tools designed to be robust for compositional data, illustrated 53 that several Prevotella spp. were prevalent in caries, while Rothia spp. were associated with the 54 health. The contributional diversity (extent to which multiple taxa contribute to each pathway) 55 of functional pathways present in the oral microbiome was decreased in the caries group. This 56 decrease was especially noticeable in several pathways known to impede caries pathogenesis, 57 including arginine and branched-chain amino acid biosynthesis. 10 host immunological markers 58 were found to be significantly elevated in the saliva of the caries group, and microbe-metabolite 59 co-occurrence analysis provided an atlas of relationships contributing to the bi-directional 60 influence between the oral microbiome and the host immune system. Finally, 527 metagenome-61 assembled genomes were obtained from the metagenomics data, representing 151 species. 23 62 taxa were novel genera/species and a further 20 taxa were novel species. This study thus serves 63 as a model analysis pipeline that will tremendously expand our knowledge of the oral microbiome 64 and its relationship to dental caries once applied to large populations. 65 67Dental caries is the most common chronic infectious disease and will afflict well over half of the 68 global human population at some point in their lives. Dental caries is particularly problematic in 69 children, where it is five times more common than asthma, the second most common chronic 70 disease. This extreme prevalence translates to an extraordinary economic burden. Caries 71 disproportionally afflicts vulnerable populations least able to access and afford proper treatment 72(1). Historically, members of the acid-producing and acid-tolerant mutans group of streptococci, 73 particularly the paradigm species of the group, Streptococcus mutans, were considered the 74 etiologic agents of the disease (2). While caries is certainly an infectious and transmissible 75 disease caused by the oral microbiota, it is now understood to be multifactorial and ecology-76 based, because although mutans streptococci are commonly associated with caries, they are 77 neither necessary nor sufficient to cause disease (3). Interplay between host genetic and 78 immunological factors, diet and hygiene habits, and the oral microbiota affect clinica...

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Section: Discussionmentioning

confidence: 60%

Section: Introductionmentioning

confidence: 99%

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

Baker

Morton

Dinis³

et al. 2019

Preprint

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“…For this, we combined our 43 MAGs with 9 human oral TM7 genomes from the literature. In addition to 3 single amplified genomes that we downloaded from the Integrated Microbial Genomes and Microbiomes database 285 (IMG/M) (Chen et al, 2019c) and refined (see Methods) and a MAG from Marcy et al (Marcy et al, 2007), we included 4 MAGs from Espinoza et al (Espinoza et al, 2018) after manually refining composite TM7 genomes (Shaiber & Eren, 2019), and the first cultivated strain of TM7, TM7x (He et al, 2015) ( Supplementary Table 7d). The phylogenomic analysis of these 52 genomes separated tongue and plaque-associated 290 genomes into distinct branches, where we could identify a single node on the tree that separated 41 of the 42 plaque associated genomes, suggesting that the site-specificity of TM7 is an ancestral trait.…”

Section: Tm7 Phylogenomic Clades Correspond To Site Of Recoverymentioning

confidence: 99%

“…Additional recent cultivation efforts are proving 120 successful in providing access to a wider variety of oral TM7 Cross et al, 2019). Recent genomeresolved and single-amplified genomics studies have also produced genomes for oral GN02 and SR1 (Campbell et al, 2013;Espinoza et al, 2018), and recently the first targeted isolation of oral SR1 strains has been reported, but genomes were not produced 125 . Despite the promise of these studies, our understanding of the ecology and evolution of these fastidious oral clades is incomplete.…”

Section: Introduction 50mentioning

confidence: 99%

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

Shaiber

Willis

Delmont

et al. 2020

Preprint

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30Microbial 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 35 tongue and dental plaque samples from multiple individuals and reconstructed 790 nonredundant 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 40 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. 45Additionally, 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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“…These results suggest that biofilm α ( Figure 1) may be associated with an increase in the abundance of biofilm formers, while biofilms β1 and β2 ( Figure 1) may be associated with a reduction in the number of biofilm formers. In agreement with this idea, the bacterial genera with higher abundance in response to anti-tick immunity include the strong biofilm formers Mycobacterium (33), Tepidimonas (34), Rothia (35) and Leuconostoc (36), whereas A. phagocytophilum infection and antimicrobial peptide reduced the presence of the biofilm formers Gracilibacteria (37) and Enterococcus (3), respectively.…”

Section: Effect Of Biological Disturbance On Taxonomic and Functionalmentioning

confidence: 69%

Resistance of tick microbiome to biological disturbance

Estrada-Peña¹,

Cabezas‐Cruz²,

Obregón³

2019

Preprint

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Background : Ixodes scapularis ticks harbor microbial communities including pathogenic and non-pathogenic microbes. Pathogen infection increases the expression of several tick gut proteins which disturb the tick gut microbiota and impact bacterial biofilm formation. Anaplasma phagocytophilum induces ticks to express I. scapularis IAFGP, a protein with antimicrobial activity while Borrelia burgdorferi induces the expression of PIXR. Here, we tested the resistance of I. scapularis microbiome to A. phagocytophilum infection, antimicrobial peptide IAFGP, and anti-tick immunity specific to PIXR. Results : We demonstrate that A. phagocytophilum infection and IAFGP affect the taxonomic composition and taxa co-occurrence networks but had no effect on the functional traits of tick microbiome. In contrast, anti-tick immunity disturbed the taxonomic composition and the functional profile of tick microbiome, by increasing both taxonomic and pathways diversity. Mechanistically, we show that anti-tick immunity increases the representation and importance of polysaccharide biosynthesis pathways involved in biofilm formation while these pathways are under-represented in the microbiome of ticks infected by A. phagocytophilum or exposed to IAFGP. Conclusions : These analyses revealed that tick microbiota is highly sensitive to anti-tick immunity, while it is less sensitive to pathogen infection and antimicrobial peptides. Results suggest that biofilm formation is a defensive response of tick microbiome to anti-tick immunity.

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Supragingival plaque microbiome ecology and functional potential in the context of health and disease

Cited by 5 publications

References 71 publications

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

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

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

Resistance of tick microbiome to biological disturbance

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