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

ABSTRACT: Tannerella forsythia and Fusobacterium nucleatum are 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 in T. 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 ?-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 ?-glucanase that cleaves glucans with ?-1,6 and ?-1,3 linkages. Furthermore, the BFO_0186-BFO_0188 locus is upregulated, with an induction of ?-glucanase activity, in cobiofilms of T. forsythia and F. nucleatum The ?-glucanase activity in mixed biofilms in turn leads to an enhanced hydrolysis of ?-glucans and release of glucose monomers and oligomers as nutrients for F. nucleatum In summary, our study highlights the role of T. forsythia ?-glucanase expressed by the asaccharolytic oral bacterium T. forsythia in the development of T. forsythia-F. nucleatum mixed species biofilms, and suggest that dietary ?-glucans might contribute in plaque development and periodontal disease pathogenesis.IMPORTANCE The 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 pathogens T. forsythia and F. nucleatum form synergistic biofilms and are closely associated in human dental plaque. In this study, we show that ?-glucanase from the periodontal pathogen T. forsythia plays a role in the formation of T. forsythia-F. nucleatum cobiofilms by hydrolyzing ?-glucans to glucose as a nutrient. We also unveiled that the expression of T. forsythia ?-glucanase is induced in response to F. nucleatum sensing. This study highlights the involvement of ?-glucanase activity in the development of T. forsythia-F. nucleatum biofilms and suggests that intake of dietary ?-glucans might be a contributing risk factor in plaque development and periodontal disease pathogenesis.

SUBMITTER: Honma K

PROVIDER: S-EPMC5734031 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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

Honma Kiyonobu K Ruscitto Angela A Sharma Ashu A

Applied and environmental microbiology 20171215 1

<i>Tannerella forsythia</i> and <i>Fusobacterium nucleatum</i> are 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 in ...[more]

PMID: 29079615

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Project description:The periodontal pathogen Tannerella forsythia expresses a β-glucanase (TfGlcA) whose expression is induced in response to Fusobacterium nucleatum, a bridge bacterium of the oral cavity. TfGlcA cleaves β-glucans to release glucose, which can serve as a carbon source for F. nucleatum and other cohabiting organisms. A two-gene cluster encoding a putative extracytoplasmic function (ECF) sigma factor and a FecR-like anti-sigma factor has been recognized upstream of a TfGlcA operon. We characterized and analyzed the role of these putative ECF sigma and anti-sigma factors in the regulation of TfGlcA expression. For this purpose, deletion mutants were constructed and analyzed for β-glucanase expression. In addition, an Escherichia coli-produced ECF sigma factor recombinant protein was evaluated for transcriptional and DNA binding activities. The results showed that the recombinant protein promoted transcription by the RNA polymerase core enzyme from the glcA promoter. Furthermore, in comparison to those in the parental strain, the β-glucanase expression levels were significantly reduced in the ECF sigma-factor deletion mutant and increased significantly in the FecR anti-sigma factor deletion mutant. The levels did not change in the mutants following coincubation with the F. nucleatum whole cells or cell extracts. Finally, the levels of β-glucanase produced by T. forsythia strains paralleled F. nucleatum biomass in cobiofilms. In conclusion, we identified a β-glucanase operon regulatory system in T. forsythia comprising an ECF sigma factor (TfSigG) and a cognate FecR-like anti-sigma factor responsive to F. nucleatum and potentially other stimuli. IMPORTANCE Previous studies have shown that F. nucleatum forms robust biofilms with T. forsythia utilizing glucose from the hydrolysis of β-glucans by T. forsythia β-glucanase, induced by F. nucleatum. In this study, we showed that a regulatory system comprising of an ECF sigma factor, TfSigG, and a FecR-like anti-sigma factor, TfFecR, is responsible for the β-glucanase induction in response to F. nucleatum, suggesting that this system plays roles in the mutualistic interactions of T. forsythia and F. nucleatum. The findings suggest the development and potential utility of small-molecule inhibitors targeting the β-glucanase activity or the TfSigG/TfFecR system as therapeutic drugs against dental plaque formation and periodontitis.

Project description:Fusobacterium nucleatum is a common oral organism that can provide adhesive and metabolic support to developing periodontal bacterial communities. It is within the context of these communities that disease occurs. We have previously reported whole cell proteomics analyses of Porphyromonas gingivalis and Streptococcus gordonii in early-stage communities with each other and with F. nucleatum, modeled using 18 h pellets. Here, we report the adaptation of F. nucleatum to the same experimental conditions as measured by differential protein expression. About 1210 F. nucleatum proteins were detected in single species F. nucleatum control samples, 1192 in communities with P. gingivalis, 1224 with S. gordonii, and 1135 with all three species. Quantitative comparisons among the proteomes revealed important changes in all mixed samples with distinct responses to P. gingivalis or S. gordonii alone and in combination. The results were inspected manually and an ontology analysis conducted using DAVID (Database for annotation, visualization, and integrated discovery). Extensive changes were detected in energy metabolism. All multispecies comparisons showed reductions in amino acid fermentation and a shift toward butanoate as a metabolic byproduct, although the two organism model community with S. gordonii showed increases in alanine, threonine, methionine, and cysteine pathways, and in the three species samples there were increases in lysine and methionine. The communities with P. gingivalis or all three organisms showed reduced glycolysis proteins, but F. nucleatum paired with S. gordonii displayed increased glycolysis/gluconeogenesis proteins. The S. gordonii containing two organism model also showed increases in the ethanolamine pathway while the three species sample showed decreases relative to the F. nucleatum single organism control. All of the nascent model communities displayed reduced translation, lipopolysaccharide, and cell wall biosynthesis, DNA replication and DNA repair.

Dataset Information

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

Publications

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

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