Characterisation of Porphyromonas gingivalis and Treponema denticola Interactions

Objectives: Porphyromonas gingivalis and Treponema denticola are synergistic partners in the aetiology of chronic periodontitis. They intimately associate in polymicrobial biofilms resulting in higher total biomass and show synergistic virulence in animal models of disease. T. denticola is a proteolytic, motile spirochaete that has unusual periplasmic flagella (FlgE) driven by an inner membrane motor (MotAB) coupled to a chemotaxis sensory system. The molecular details of its virulence are poorly characterised due to limitations in its genetic manipulation. P. gingivalis is a highly proteolytic, sessile bacterium. Coculture of P. gingivalis and T. denticola resulted in upregulation of T. denticola glycine catabolic pathways, while P. gingivalis growth in T. denticola conditioned medium (TdCM) increased free glycine production, the preferred energy source for T. denticola.
Methods: To examine the interactions between T. denticola and P. gingivalis that result in enhanced polymicrobial biofilm formation and development a series of P. gingivalis and T. denticola mutants were created. T. denticola flgE-, motA- and motB- mutants all had impaired motility relative to the wild-type.
Results: The motA- and motB- mutants, but not flgE-, had similar coaggregation rates with P. gingivalis compared with the wild-type. T. denticola motility mutants had reduced ability to incorporate into polymicrobial biofilms with P. gingivalis. P. gingivalis aminopeptidase (PG1605-) and cysteine peptidase (PG1788-) mutants displayed reductions in free glycine production in TdCM, relative to wild-type. RNA-Seq analysis of P. gingivalis growing in TdCM showed that a range of metabolic pathways were differentially regulated, including significant upregulation of succinate catabolic pathways, supporting the cross feeding of succinate by T. denticola to P. gingivalis.
Conclusions: This work provides insights into the mechanisms involved between P. gingivalis and T. denticola to increase their growth and fitness advantage in a complex disease-associated community.