Effect of Periodontal Pathogens on the Metatranscriptome of a Healthy Multispecies Biofilm Model

Frias-Lopez, Jorge; Duran-Pinedo, Ana E.

doi:10.1128/jb.06328-11

Cited by 89 publications

(87 citation statements)

References 85 publications

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“…Notably, functions related to bacterial motility, energy metabolism, lipopolysaccharide (LPS) biosynthesis, flagellar assembly, methane metabolism, bacterial chemotaxis, and peptidases were abundant in chronic periodontitis cases. These results are consistent with recent metagenomic data (34,53). Going forward, elucidating the role of key bacteria encoding these functions and understanding the basis of individual variations in microbiomes and metagenomes will be essential in future studies.…”

Section: Discussionsupporting

confidence: 78%

Dysbiosis and Alterations in Predicted Functions of the Subgingival Microbiome in Chronic Periodontitis

Kirst

Alfant

et al. 2015

Appl Environ Microbiol

191

188

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Chronic periodontitis is an inflammatory disease of the periodontium affecting nearly 65 million adults in the United States. Changes in subgingival microbiota have long been associated with chronic periodontitis. Recent culture-independent molecular studies have revealed the immense richness and complexity of oral microbial communities. However, data sets across studies have not been directly compared, and whether the observed microbial variations are consistent across different studies is not known. Here, we used 16S rRNA sequencing to survey the subgingival microbiota in 25 subjects with chronic periodontal disease and 25 healthy controls and compared our data sets with those of three previously reported microbiome studies. Consistent with data from previous studies, our results demonstrate a significantly altered microbial community structure with decreased heterogeneity in periodontal disease. Comparison with data from three previously reported studies revealed that subgingival microbiota clustered by study. However, differences between periodontal health and disease were larger than the technical variations across studies. Using a prediction score and applying five different distance metrics, we observed two predominant clusters. One cluster was driven by Fusobacterium and Porphyromonas and was associated with clinically apparent periodontitis, and the second cluster was dominated by Rothia and Streptococcus in the majority of healthy sites. The predicted functional capabilities of the periodontitis microbiome were significantly altered. Genes involved in bacterial motility, energy metabolism, and lipopolysaccharide biosynthesis were overrepresented in periodontal disease, whereas genes associated with transporters, the phosphotransferase system, transcription factors, amino acid biosynthesis, and glycolysis/gluconeogenesis were enriched in healthy controls. These results demonstrate significant alterations in microbial composition and function in periodontitis and suggest genes and metabolic pathways associated with periodontal disease. P eriodontal disease is a common disease affecting many adults in the United States. If left untreated, chronic periodontitis (CP) can lead to serious problems such as tooth loss. Indeed, periodontal disease is the number one cause of tooth loss in the United States, accounting for half of all tooth loss in U.S. adults (1). There is considerable evidence that the clinical impact of periodontal disease extends beyond the oral cavity (2). Strong associations have been found between periodontitis and a number of systemic conditions, including cardiovascular disease (3, 4), preterm delivery and low-birth-weight babies (5), diabetes mellitus (6-8), and rheumatoid arthritis (9-11).The activity of periodontal disease is determined by a complex interplay between the immune system and periodontal pathogens (12, 13). Alterations in subgingival microbiota have long been associated with the development and progression of periodontitis (14). In susceptible individuals, perturbations in...

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Section: Discussionsupporting

confidence: 78%

Dysbiosis and Alterations in Predicted Functions of the Subgingival Microbiome in Chronic Periodontitis

Kirst

Alfant

et al. 2015

Appl Environ Microbiol

191

188

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“…The metatranscriptome refers to the gene expression of the whole microbial community [12]. Previous studies have shown differences in microbial gene expression based on sample site within the oral cavity [13] between health and periodontitis [14] and dental caries [15,16].…”

Section: Introductionmentioning

confidence: 99%

Functional profiles of coronal and dentin caries in children

Kressirer

Chen

Harriman³

et al. 2018

Journal of Oral Microbiology

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Background: Dental caries results from a dysbiosis of tooth-associated biofilms and frequently extends through enamel into dentin which has a different structure and composition.Objective: To evaluate the metatranscriptome of caries to determine the metabolic potential of caries communities compared with health.Design: Samples from children, caries-free (CF: n = 4) or with coronal (CC: n = 5) or dentin (DC: n = 5) caries were examined for gene expression potential. Functional profiling was performed using HUMAnN2 (HMP Unified Metabolic Analysis Network).Results: There was increased gene expression diversity in DC compared with CC and CF. Genes in CF included alcohol dehydrogenase from Neisseria sicca, methylenetetrahydrofolate reductase from Streptococcus sanguinis and choline kinase from streptococci. Genes in CC mapped mainly to Streptococcus mutans. Arginine deiminase in DC mapped to S. sanguinis and Actinomyces naeslundii. Glycerol kinase genes mapped to S. sanguinis in all groups whereas glycerol kinase in DC were from Rothia, Prevotella and streptococci. Uracil-DNA glycosylase in DC mapped to Prevotella denticola and Actinomyces. Repressor LexA in DC mapped to Scardovia wiggsiae, Dialister invisus and Veillonella parvula.Conclusions: Functional profiling revealed enzyme activities in both caries and caries-free communities and clarified marked differences between coronal and dentin caries in bacterial composition and potential gene expression.

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“…We had previously observed the upregulation of putative transposases in an S. mitis biofilm in a multispecies biofilm model where two periodontal pathogens (P. gingivalis and A. actinomycetemcomitans) were added simultaneously (8). We first verified the upregulation of these putative transposases when only P. gingivalis was added.…”

Section: Resultsmentioning

confidence: 83%

“…As mentioned above, in a previous metatranscriptomic analysis we observed a high upregulation of a large number of putative trans-posases in S. mitis expression profiles when P. gingivalis and Aggregatibacter actinomycetemcomitans were added to an established healthy biofilm (8). Upregulation of putative transposases has been observed by Mitchell et al in the periodontal pathogen T. denticola when growing as a biofilm but not in planktonic growth, concluding that there is a higher potential for genetic mobility in T. denticola biofilms (16).…”

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confidence: 90%

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The Periodontal Pathogen Porphyromonas gingivalis Induces Expression of Transposases and Cell Death of Streptococcus mitis in a Biofilm Model

Duran-Pinedo¹,

Baker²,

Frias-Lopez

2014

Infect Immun

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Oral microbial communities are extremely complex biofilms with high numbers of bacterial species interacting with each other (and the host) to maintain homeostasis of the system. Disturbance in the oral microbiome homeostasis can lead to either caries or periodontitis, two of the most common human diseases. Periodontitis is a polymicrobial disease caused by the coordinated action of a complex microbial community, which results in inflammation of tissues that support the teeth. It is the most common cause of tooth loss among adults in the United States, and recent studies have suggested that it may increase the risk for systemic conditions such as cardiovascular diseases. In a recent series of papers, Hajishengallis and coworkers proposed the idea of the "keystone-pathogen" where low-abundance microbial pathogens (Porphyromonas gingivalis) can orchestrate inflammatory disease by turning a benign microbial community into a dysbiotic one. The exact mechanisms by which these pathogens reorganize the healthy oral microbiome are still unknown. In the present manuscript, we present results demonstrating that P. gingivalis induces S. mitis death and DNA fragmentation in an in vitro biofilm system. Moreover, we report here the induction of expression of multiple transposases in a Streptococcus mitis biofilm when the periodontopathogen P. gingivalis is present. Based on these results, we hypothesize that P. gingivalis induces S. mitis cell death by an unknown mechanism, shaping the oral microbiome to its advantage.T he human oral microbiome consists of over 600 individual taxa (1, 2). Its complexity and the fact that a large fraction of species is noncultivable have hampered our knowledge of the molecular and metabolic interactions that occur between the species of the bacterial biofilm and between bacteria and host.Periodontal disease is a polymicrobial inflammatory biofilm-mediated pathology that leads to a progressive loosening and eventual loss of teeth (3, 4), and it is responsible for half of all tooth loss in adults that occurs in moderate form in 39% of American adults and in severe form in 9% of adults. Polymicrobial diseases are increasingly being recognized as more frequent than previously thought (5). In these diseases there are complex interactions among the etiologic agents, which ultimately lead to disease. In the microbial etiology of periodontitis it is generally accepted that a consortium of bacteria, not a single microorganism, is involved in the disease. Nonetheless, it is well established that in destructive periodontitis, the "red complex" (Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia) are key players in the disease process (6).A more holistic treatment of periodontitis or any other polymicrobial disease requires a better understanding of the ecology of the microbial community and the mechanisms that cause the shift from a mature stable biofilm to a dysbiotic community responsible for disease. Maintaining a healthy biofilm would be a less invasive strategy than removing an ...

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Effect of Periodontal Pathogens on the Metatranscriptome of a Healthy Multispecies Biofilm Model

Cited by 89 publications

References 85 publications

Dysbiosis and Alterations in Predicted Functions of the Subgingival Microbiome in Chronic Periodontitis

Dysbiosis and Alterations in Predicted Functions of the Subgingival Microbiome in Chronic Periodontitis

Functional profiles of coronal and dentin caries in children

The Periodontal Pathogen Porphyromonas gingivalis Induces Expression of Transposases and Cell Death of Streptococcus mitis in a Biofilm Model

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