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.
Highlights
Chronic periodontitis is an inflammatory disease of the supporting tissues of the teeth with a polymicrobial aetiology
We showed that the sum of the interactions between P. gingivalis and T. denticola resulted in sustained interspecies growth symbiosis in continuous culture over an extended time frame
A dual species transcriptome analysis determined that T. denticola and P. gingivalis responded to each other in co-culture by altering the expression of a substantial proportion of genes, notably those involved in T. denticola metabolism and virulence
Summary
Chronic periodontitis is an inflammatory disease of the supporting tissues of the teeth with a polymicrobial aetiology. We have previously demonstrated in a longitudinal human study that the imminent progression of chronic periodontitis in patients on a maintenance program could be predicted by increases in the relative proportions of P. gingivalis and/or T. denticola in subgingival plaque above threshold levels [6]. P. gingivalis and T. denticola responded to each other’s presence in a polymicrobial biofilm by modulating the abundance of a range of proteins [26] Together these data suggest there is an intimate relationship between these two species that has evolved to enhance their survival and virulence. The physiochemical interactions that result in the observed symbiotic and synergistic effects during P. gingivalis and T. denticola co-culture remain largely unknown
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