The chronicles of Porphyromonas gingivalis: the microbium, the human oral epithelium and their interplay

Abstract

The microbiota of the human oral mucosa consists of a myriad of bacterial species that normally exist in commensal harmony with the host. Porphyromonas gingivalis, an aetiological agent in severe forms of periodontitis (a chronic inflammatory disease), is a prominent component of the oral microbiome and a successful colonizer of the oral epithelium. This Gram-negative anaerobe can also exist within the host epithelium without the existence of overt disease. Gingival epithelial cells, the outer lining of the gingival mucosa, which function as an important part of the innate immune system, are among the first host cells colonized by P. gingivalis. This review describes recent studies implicating the co-existence and intracellular adaptation of the organism in these target host cells. Specifically, recent findings on the putative mechanisms of persistence, intercellular dissemination and opportunism are highlighted. These new findings may also represent an original and valuable model for mechanistic characterization of other successful host-adapted, self-limiting, persistent intracellular bacteria in human epithelial tissues.

Fig. 1

(a) Intercellular translocation of P. gingivalis through actin fibres at 24 h post-infection visualized by immunofluorescence microscopy. The actin cytoskeleton is stained red and P. gingivalis is green. DAPI (blue) was used to stain the nuclei to determine the localization of P. gingivalis in the cytoplasm. The white arrow indicates actin projections and bacterial translocation between the host cells. Bar, 10 µm. [This panel is reproduced from Yilmaz et al. (2006) with permission from the American Society for Microbiology.] (b) P. gingivalis spreading visualized by immunofluorescence microscopy. After 24 h co-incubation of initially 24 h-infected cells (blue) with initially uninfected cells (green), transmission of P. gingivalis to newly infected cells (green) can be seen, displaying red-labelled P. gingivalis in their cytosol. White arrows indicate newly infected cells. Bar, 10 µm.

Fig. 2

Three-dimensional confocal scanning fluorescence microscopy showing a 24 h-infected primary GEC (actin, red; nuclei, blue) with high numbers of intracellular P. gingivalis (green) undergoing successful mitosis. White arrows indicate the infected cell producing two daughter nuclei. Bar 10 µm.