Treponema denticola improves adhesive capacities of Porphyromonas gingivalis

Abstract

Porphyromonas gingivalis, an important etiological agent of periodontal disease, is frequently found associated with Treponema denticola, an anaerobic spirochete, in pathogenic biofilms. However, interactions between these two bacteria are not well understood at the molecular level. In this study, we seek to link the influence of T. denticola on the expression of P. gingivalis proteases with its capacities to adhere and to form biofilms. The P. gingivalis genes encoding Arg-gingipain A (RgpA), Lys-gingipain (Kgp), and hemagglutinin A (HagA) were more strongly expressed after incubation with T. denticola compared with P. gingivalis alone. The amounts of the three resulting proteins, all of which contain hemagglutinin adhesion domains, were increased in culture supernatants. Moreover, incubation of P. gingivalis with T. denticola promoted static and dynamic biofilm formation, primarily via a time-dependent enhancement of P. gingivalis adhesion capacities on bacterial partners such as Streptococcus gordonii. Adhesion of P. gingivalis to human cells was also increased. These results showed that interactions of P. gingivalis with other bacterial species, such as T. denticola, induce increased adhesive capacities on various substrata by hemagglutinin adhesion domain-containing proteins.

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“…P. gingivalis produces isobutyric acid which stimulates growth of the oral spirochete Treponema denticola , while T. denticola produces succinic acid which enhances growth of P. gingivalis [8]. Contact with T. denticola also upregulates the expression of P. gingivalis adhesins and proteases [9]. Consequently, growth of P. gingivalis and T. denticola in a dual species biofilm produces a significantly larger biomass compared to the total of the individual monospecies biofilms, and the organisms are synergistically pathogenic in murine models of periodontal disease [8, 10].…”

Intercellular communications in multispecies oral microbial communities

“…Meanwhile, signaling can also be triggered when different bacterial species are in direct physical contact. P. gingivalis was reported to acquire increased adhesive capacities on various substrata through up-regulated expression of gingipain upon contact with T. denticola (Meuric et al, 2013). The transcriptional responses as a result of cell–cell contact often are not limited to a few genes.…”

Recent Advances in Studies of Polymicrobial Interactions in Oral Biofilms

“…Differentially expressed genes in the dual-species environment have been mainly involved in metabolism and energy production, but also potential virulence factors such as a tyrosine phosphatase [19,46]. Similar studies have demonstrated that co-culture with T. denticola promoted increased expression of P. gingivalis adhesin genes and proteases [59]. In contrast, a negative interaction was found between P. gingivalis and S. cristatus that downregulated expression of P. gingivalis fimbrial (fimA) genes, and interfering with biofilm formation [92].…”

“…Mixed communities of Streptococcus and Veillonella species, micromanipulated from dental plaque, have been developed using saliva as a sole source of nutrients [57]. More recently, these model systems have been used to identify new mechanisms of co-operation involving protease interactions between T. denticola and P. gingivalis [58,59] and AI-2 signalling between S. gordonii and C. albicans [42]. [37].…”

“…Simple biofilm models comprising two or three species have proved to be an excellent method to determine individual inter-species relationships [61] [58,59] [62] [35]. However, many interactions are complex and involve multiple community members.…”