scholarly journals β-Glucanase Activity of the Oral Bacterium Tannerella forsythia Contributes to the Growth of a Partner Species, Fusobacterium nucleatum, in Cobiofilms

2017 ◽  
Vol 84 (1) ◽  
Author(s):  
Kiyonobu Honma ◽  
Angela Ruscitto ◽  
Ashu Sharma

ABSTRACTTannerella forsythiaandFusobacterium nucleatumare dental plaque bacteria implicated in the development of periodontitis. These two species have been shown to form synergistic biofilms and have been found to be closely associated in dental plaque biofilms. A number of genetic loci for TonB-dependent membrane receptors (TDR) for glycan acquisition, with many existing in association with genes coding for enzymes involved in the breakdown of complex glycans, have been identified inT. forsythia. In this study, we focused on a locus, BFO_0186-BFO_0188, that codes for a predicted TDR-SusD transporter along with a putative β-glucan hydrolyzing enzyme (BFO_0186). This operon is located immediately downstream of a 2-gene operon that codes for a putative stress-responsive extracytoplasmic function (ECF) sigma factor and an anti-sigma factor. Here, we show that BFO_0186 expresses a β-glucanase that cleaves glucans with β-1,6 and β-1,3 linkages. Furthermore, the BFO_0186-BFO_0188 locus is upregulated, with an induction of β-glucanase activity, in cobiofilms ofT. forsythiaandF. nucleatum. The β-glucanase activity in mixed biofilms in turn leads to an enhanced hydrolysis of β-glucans and release of glucose monomers and oligomers as nutrients forF. nucleatum. In summary, our study highlights the role ofT. forsythiaβ-glucanase expressed by the asaccharolytic oral bacteriumT. forsythiain the development ofT. forsythia-F. nucleatummixed species biofilms, and suggest that dietary β-glucans might contribute in plaque development and periodontal disease pathogenesis.IMPORTANCEThe development of dental plaque biofilm is a complex process in which metabolic, chemical and physical interactions between bacteria take a central role. Previous studies have shown that the dental pathogensT. forsythiaandF. nucleatumform synergistic biofilms and are closely associated in human dental plaque. In this study, we show that β-glucanase from the periodontal pathogenT. forsythiaplays a role in the formation ofT. forsythia-F. nucleatumcobiofilms by hydrolyzing β-glucans to glucose as a nutrient. We also unveiled that the expression ofT. forsythiaβ-glucanase is induced in response toF. nucleatumsensing. This study highlights the involvement of β-glucanase activity in the development ofT. forsythia-F. nucleatumbiofilms and suggests that intake of dietary β-glucans might be a contributing risk factor in plaque development and periodontal disease pathogenesis.

2009 ◽  
Vol 191 (22) ◽  
pp. 6804-6811 ◽  
Author(s):  
Saravanan Periasamy ◽  
Paul E. Kolenbrander

ABSTRACT Porphyromonas gingivalis is present in dental plaque as early as 4 h after tooth cleaning, but it is also associated with periodontal disease, a late-developing event in the microbial successions that characterize daily plaque development. We report here that P. gingivalis ATCC 33277 is remarkable in its ability to interact with a variety of initial, early, middle, and late colonizers growing solely on saliva. Integration of P. gingivalis into multispecies communities was investigated by using two in vitro biofilm models. In flow cells, bacterial growth was quantified using fluorescently conjugated antibodies against each species, and static biofilm growth on saliva-submerged polystyrene pegs was analyzed by quantitative real-time PCR using species-specific primers. P. gingivalis could not grow as a single species or together with initial colonizer Streptococcus oralis but showed mutualistic growth when paired with two other initial colonizers, Streptococcus gordonii and Actinomyces oris, as well as with Veillonella sp. (early colonizer), Fusobacterium nucleatum (middle colonizer), and Aggregatibacter actinomycetemcomitans (late colonizer). In three-species flow cells, P. gingivalis grew with Veillonella sp. and A. actinomycetemcomitans but not with S. oralis and A. actinomycetemcomitans. Also, it grew with Veillonella sp. and F. nucleatum but not with S. oralis and F. nucleatum, indicating that P. gingivalis and S. oralis are not compatible. However, P. gingivalis grew in combination with S. gordonii and S. oralis, demonstrating its ability to overcome the incompatibility when cultured with a second initially colonizing species. Collectively, these data help explain the observed presence of P. gingivalis at all stages of dental plaque development.


2021 ◽  
Vol 67 (2) ◽  
pp. 128-134
Author(s):  
Cristina Vodiță ◽  
◽  
Doina Lucia Ghergic ◽  
Emanuel Alin Vodiță ◽  
Raluca Monica Comăneanu ◽  
...  

Objectives. The study aimed to detect the presence/quantification of the 12 bacterial strains more frequently involved in the occurrence and aggravation of periodontal disease in a group of patients. Material and method. The study included 55 patients of both sexes, from the portfolio of the „Dr. Vodiță“ Dental Clinic, with chronic marginal periodontitis, who had not been under regular dental control and hygiene for at least 2 years. During the first treatment session, fluid was collected from each patient from the periodontal bags using sterile paper cones from the collection putty. Subsequently, fluid-soaked paper cones from periodontal bags were sent to the Genetic Lab in Bucharest for DNA extraction and quantification of 12 bacterial species, more common in the etiology of periodontal disease. For the correctness of the results obtained, it is necessary that patients have not taken antibiotics in the last 3 weeks. The data were analyzed and statistically processed with the Microsoft Excel 2016 program. Results. The least common bacteria found were from the species: Capnocytophaga ochracea, Aggregatibacter actinomycetemcomitans, Eikanella corrodens and Campylobacter rectus, closely followed by Capnocytophaga gingivalis, Prevotella intermedia and Capnocytophaga sputigena. The rest of the bacterial species were detected much more frequently. Discussions. In the analyzed group there was no monoinfection with Aggregatibacter actinomycetemcomitans. Porphyromonas gingivalis had an important presence in the studied group, registering increased levels in 89% of cases. In our group, Treponema denticola was present in increased amounts in 76.36% of cases. Tannerella forsythia was present in 92.72% of cases in elevated concentrations. Eikanella corrodens and Campylobacter rectus were present in 18.18% of the cases studied in high quantities. Prevotella intermedia was present in significant amounts in 34.54% of cases. Fusobacterium nucleatum was present in high concentrations in 98.18% of the cases studied. Prevotella nigrescens was present in increased amounts in 56.36% of cases. Capnocytophaga ochracea was present in 9.09% of cases in high amounts, Capnocytophaga sputigena in 38.18% of cases, and Capnocytophaga gingivalis was detected in 24.45% of cases. Conclusions. From the class of bacteria with high pathogenicity, we most frequently encountered in the studied group Tannerella forsythia. From the class of bacteria with moderate pathogenicity, we encountered the most common Fusobacterium nucleatum. From the class of bacteria with low pathogenicity, we encountered the most common Capnocytophaga sputigena. In order to validate the results obtained, it is necessary to extend the study to a larger number of patients.


2000 ◽  
Vol 68 (4) ◽  
pp. 1893-1898 ◽  
Author(s):  
Anahid Jewett ◽  
Wyatt R. Hume ◽  
Ho Le ◽  
Tri N. Huynh ◽  
Yiping W. Han ◽  
...  

ABSTRACT It is largely unknown why a variety of bacteria present in the oral cavity are capable of establishing themselves in the periodontal pockets of nonimmunocompromised individuals in the presence of competent immune effector cells. In this paper we present evidence for the immunosuppressive role of Fusobacterium nucleatum, a gram-negative oral bacterium which plays an important role in the generation of periodontal disease. Our studies indicate that the immunosuppressive role of F. nucleatum is largely due to the ability of this organism to induce apoptotic cell death in peripheral blood mononuclear cells (PBMCs) and in polymorphonuclear cells (PMNs). F. nucleatum treatment induced apoptosis of PBMCs and PMNs as assessed by an increase in subdiploid DNA content determined by DNA fragmentation and terminal deoxynucleotidyltransferase-mediated dUTP-biotin nick end-labeling assays. The ability of F. nucleatum to induce apoptosis was abolished by either heat treatment or proteinase digestion but was retained after formaldehyde treatment, suggesting that a heat-labile surface protein component is responsible for bacterium-mediated cell apoptosis. The data also indicated that F. nucleatum-induced cell apoptosis requires activation of caspases and is protected by NF-κB. Possible mechanisms of F. nucleatum's role in the pathogenesis of periodontal disease are discussed.


2017 ◽  
Vol 5 (46) ◽  
Author(s):  
Richard D. Haigh ◽  
Liam A. Crawford ◽  
Joseph D. Ralph ◽  
Joseph J. Wanford ◽  
Sonia R. Vartoukian ◽  
...  

ABSTRACT Periodontal disease comprises mild to severe inflammatory host responses to oral bacteria that can cause destruction of the tooth-supporting tissue. We report genome sequences for 18 clinical isolates of Porphyromonas gingivalis, Prevotella intermedia, and Tannerella forsythia, Gram-negative obligate anaerobes that play a role in the periodontal disease process.


2013 ◽  
Vol 81 (4) ◽  
pp. 1198-1206 ◽  
Author(s):  
Naohiro Shimotahira ◽  
Yuichi Oogai ◽  
Miki Kawada-Matsuo ◽  
Sakuo Yamada ◽  
Kenji Fukutsuji ◽  
...  

ABSTRACTTannerella forsythiais an anaerobic, Gram-negative bacterium involved in the so-called “red complex,” which is associated with severe and chronic periodontitis. The surface layer (S-layer) ofT. forsythiais composed of cell surface glycoproteins, such as TfsA and TfsB, and is known to play a role in adhesion/invasion and suppression of proinflammatory cytokine expression. Here we investigated the association of this S-layer with serum resistance and coaggregation with other oral bacteria. The growth of the S-layer-deficient mutant in a bacterial medium containing more than 20% non-heat-inactivated calf serum (CS) or more than 40% non-heat-inactivated human serum was significantly suppressed relative to that of the wild type (WT). Next, we used confocal microscopy to perform quantitative analysis on the effect of serum. The survival ratio of the mutant exposed to 100% non-heat-inactivated CS (76% survival) was significantly lower than that of the WT (97% survival). Furthermore, significant C3b deposition was observed in the mutant but not in the WT. In a coaggregation assay, the mutant showed reduced coaggregation withStreptococcus sanguinis,Streptococcus salivarius, andPorphyromonas gingivalisbut strong coaggregation withFusobacterium nucleatum. These results indicated that the S-layer ofT. forsythiaplays multiple roles in virulence and may be associated with periodontitis.


mSphere ◽  
2021 ◽  
Author(s):  
Paul D. Veith ◽  
Nichollas E. Scott ◽  
Eric C. Reynolds

Tannerella forsythia is an oral pathogen associated with severe forms of periodontal disease characterized by destruction of the tooth’s supporting tissues, including the bone. The bacterium releases a variety of proteins associated with virulence on the surface of outer membrane vesicles.


2020 ◽  
Vol 11 (2) ◽  
pp. 165-171
Author(s):  
Fatih Karaaslan ◽  
Turgut Demir ◽  
Ozlem Barış

Aim: To investigate whether bacteria that play a major role in periodontal disease pathology and in the formation of dental plaque also affect the formation of dental calculus, which is a predisposing factor for the initiation and progression of periodontal diseases. Materials and Methods: This was an in vitro study, and cultures of bacteria were obtained from the American Type Culture Collection and Department of Biology, Faculty of Science, Atatürk University. Young cultures of bacteria of Streptococcus mutans ( S. mutans), Streptococcus sanguinis ( S. sanguinis), Streptococcus gordonii ( S. gordonii), Aggregatibacter actinomycetemcomitans ( A. actinomycetemcomitans), Porphyromonas gingivalis ( P. gingivalis), Fusobacterium nucleatum ( F. nucleatum), and Corynebacterium matruchotii ( C. matruchotii) were prepared in media containing their specific enriching factors. B2 solid, B4 solid, and B2 liquid media were used to determine active calcification, whereas the mineral salt basal (MSB) medium was used to observe passive calcification. Calcification in the media was measured under light microscopy and in MSB using a spectrophotometer and was recorded as the percent transmittance. Results: S. mutans, S. sanguinis, and S. gordonii showed calcification in the B2 medium. S. mutans, S. sanguinis, S. gordonii, and C. matruchotii demonstrated calcification in MSB. A. actinomycetemcomitans, P. gingivalis, and F. nucleatum did not show any calcification. Conclusions: It was concluded that streptococci present in dental plaque take part in the formation of dental calculus, whereas periodontopathogens have no role in the formation of dental calculus.


2012 ◽  
Vol 80 (7) ◽  
pp. 2436-2443 ◽  
Author(s):  
Rajendra P. Settem ◽  
Ahmed Taher El-Hassan ◽  
Kiyonobu Honma ◽  
Graham P. Stafford ◽  
Ashu Sharma

ABSTRACTTannerella forsythiais strongly associated with chronic periodontitis, an inflammatory disease of the tooth-supporting tissues, leading to tooth loss.Fusobacterium nucleatum, an opportunistic pathogen, is thought to promote dental plaque formation by serving as a bridge bacterium between early- and late-colonizing species of the oral cavity. Previous studies have shown thatF. nucleatumspecies synergize withT. forsythiaduring biofilm formation and pathogenesis. In the present study, we showed that coinfection ofF. nucleatumandT. forsythiais more potent than infection with either species alone in inducing NF-κB activity and proinflammatory cytokine secretion in monocytic cells and primary murine macrophages. Moreover, in a murine model of periodontitis, mixed infection with the two species induces synergistic alveolar bone loss, characterized by bone loss which is greater than the additive alveolar bone losses induced by each species alone. Further, in comparison to the single-species infection, mixed infection caused significantly increased inflammatory cell infiltration in the gingivae and osteoclastic activity in the jaw bones. These data show thatF. nucleatumsubspecies andT. forsythiasynergistically stimulate the host immune response and induce alveolar bone loss in a murine experimental periodontitis model.


2012 ◽  
Vol 78 (16) ◽  
pp. 5638-5645 ◽  
Author(s):  
Yoon-Suk Kang ◽  
Brian Bothner ◽  
Christopher Rensing ◽  
Timothy R. McDermott

ABSTRACTIn this study with the model organismAgrobacterium tumefaciens, we used a combination oflacZgene fusions, reverse transcriptase PCR (RT-PCR), and deletion and insertional inactivation mutations to show unambiguously that the alternative sigma factor RpoN participates in the regulation of AsIIIoxidation. A deletion mutation that removed the RpoN binding site from theaioBApromoter and anaacC3(gentamicin resistance) cassette insertional inactivation of therpoNcoding region eliminatedaioBAexpression and AsIIIoxidation, althoughrpoNexpression was not related to cell exposure to AsIII. Putative RpoN binding sites were identified throughout the genome and, as examples, included promoters foraioB,phoB1,pstS1,dctA,glnA,glnB, andflgBthat were examined by using qualitative RT-PCR andlacZreporter fusions to assess the relative contribution of RpoN to their transcription. The expressions ofaioBanddctAin the wild-type strain were considerably enhanced in cells exposed to AsIII, and both genes were silent in therpoN::aacC3mutant regardless of AsIII. The expression level ofglnAwas not influenced by AsIIIbut was reduced (but not silent) in therpoN::aacC3mutant and further reduced in the mutant under N starvation conditions. TherpoN::aacC3mutation had no obvious effect on the expression ofglnB,pstS1,phoB1, orflgB. These experiments provide definitive evidence to document the requirement of RpoN for AsIIIoxidation but also illustrate that the presence of a consensus RpoN binding site does not necessarily link the associated gene with regulation by AsIIIor by this sigma factor.


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