Porphyromonas gingivalis and Treponema denticola exhibit metabolic symbioses

PLoS Pathog. 2014 Mar 6;10(3):e1003955. doi: 10.1371/journal.ppat.1003955. eCollection 2014 Mar.

Abstract

Porphyromonas gingivalis and Treponema denticola are strongly associated with chronic periodontitis. These bacteria have been co-localized in subgingival plaque and demonstrated to exhibit symbiosis in growth in vitro and synergistic virulence upon co-infection in animal models of disease. Here we show that during continuous co-culture a P. gingivalis:T. denticola cell ratio of 6∶1 was maintained with a respective increase of 54% and 30% in cell numbers when compared with mono-culture. Co-culture caused significant changes in global gene expression in both species with altered expression of 184 T. denticola and 134 P. gingivalis genes. P. gingivalis genes encoding a predicted thiamine biosynthesis pathway were up-regulated whilst genes involved in fatty acid biosynthesis were down-regulated. T. denticola genes encoding virulence factors including dentilisin and glycine catabolic pathways were significantly up-regulated during co-culture. Metabolic labeling using 13C-glycine showed that T. denticola rapidly metabolized this amino acid resulting in the production of acetate and lactate. P. gingivalis may be an important source of free glycine for T. denticola as mono-cultures of P. gingivalis and T. denticola were found to produce and consume free glycine, respectively; free glycine production by P. gingivalis was stimulated by T. denticola conditioned medium and glycine supplementation of T. denticola medium increased final cell density 1.7-fold. Collectively these data show P. gingivalis and T. denticola respond metabolically to the presence of each other with T. denticola displaying responses that help explain enhanced virulence of co-infections.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Coculture Techniques
  • Coinfection
  • Microscopy, Electron, Scanning
  • Oligonucleotide Array Sequence Analysis
  • Porphyromonas gingivalis / genetics
  • Porphyromonas gingivalis / growth & development
  • Porphyromonas gingivalis / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Symbiosis / physiology*
  • Transcriptome
  • Treponema denticola / genetics
  • Treponema denticola / growth & development
  • Treponema denticola / metabolism*

Grants and funding

This work was supported by the Australian National Health and Medical Research Council Project Grant Number 1008061. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.