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

Abstract

and are dental plaque bacteria implicated in the development of periodontitis. These two species have been shown to form synergistic biofilms and 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 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 two-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 -1, 3 linkages. Furthermore, BFO_0186-BFO_0188 locus is upregulated, with an induction of β-glucanase activity, in co-biofims of and 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 for In summary, our study highlights the role of β-glucanase expressed by the asaccharolytic oral bacterium in the development of mixed species biofilms, and suggest that dietary β-glucans might contribute in plaque development and periodontal disease pathogenesis. 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 pathogen and form synergistic biofilms and are closely associated in the human dental plaque. In this study, we show that β-glucanase from the periodontal pathogen plays a role in the formation of co-biofilms by hydrolyzing β-glucans to glucose as a nutrient. We also unveiled that the expression of β-glucanase is induced in response to sensing. This study highlights the involvement of β-glucanase activity in the development of biofilms, and suggest that intake of dietary β-glucans might be a contributing risk factor in plaque development and periodontal disease pathogenesis.

Potential Microbiological Risk Factors Associated With Periodontitis and Periodontal Health Disparities

“…A recent clinical study used immunohistochemistry and qPCR to show that P. gingivalis and T. forsythia aggregated in dental plaques and periodontal tissues from periodontitis patients ( Rajakaruna et al., 2018 ). The interaction between F. nucleatum and T. forsythia is well established; it likely involves the hydrolyzation of β-glucans by T. forsythia β-glucanase ( Sharma et al., 2005 ; Honma et al., 2018 ). However, direct interaction between T. forsythia and T. denticola has not been revealed.…”

Broad geographical and ecological diversity from similar genomic toolkits in the ascomycete genusTetracladium

“…As was the case for S. sclerotiorum and B. cinerea when enrichment for GH71 in these fungi was first reported, it is unknown whether the abundant α-1,3-glucanases in these genomes is associated degradation of the fungi’s own cell walls or those of antagonistic fungi(101), or whether these enzymes play other roles entirely. Interestingly, α-1,3-glucan is important in the matrix of fungal and bacterial biofilms (102) which can be disrupted by glucanases (103, 104). Decomposing leaves in streams and the roots of plants are covered by microbial biofilms and it is possible that enrichment for α -1,3-glucanase in Tetracladium genomes is associated with interactions with those biofilms.…”

Microbiome and morbid obesity increase pathogenic stimulus diversity

“…Oral microbiome composition alters fatty acid metabolism [12] and are not just associated with oral cancer development [13] but also are suspected of promoting esophageal [14,15], pancreatic cancer [16,17], or liver cancer [18]. T. forsythia "contributes to the growth of a partner species, Fusobacterium nucleatum, in co-biofilms" [19]. F. nucleatum is associated with the precancerous serrated adenoma of the proximal colon [20] and various cancers [21,22].…”