The periodontopathogen Porphyromonas gingivalis binds iron protoporphyrin IX in the μ-oxo dimeric form: an oxidative buffer and possible pathogenic mechanism

Abstract

Mössbauer spectroscopy was used to re-evaluate iron protoporphyrin IX, FePPIX, binding and the chemical nature of the black iron porphyrin pigment of Porphyromonas gingivalis. We demonstrate that FePPIX is bound to the cell in the µ-oxo dimeric form, [Fe(III)PPIX]2O, and that the iron porphyrin pigment is also composed of this material. P. gingivalis also assimilated monomeric Fe(II)- and Fe(III)PPIX into µ-oxo dimers in vitro. Scatchard analysis revealed a greater binding maximum of cells for µ-oxo dimers than for monomeric Fe(III)-or Fe(II)PPIX, although the relative affinity constant for the dimers was lower. Formation of [Fe(III)PPIX]2O via reactions of Fe(II)PPIX with oxygen, and its toxic derivatives, would serve as an oxidative buffer and permit P. gingivalis and other black-pigmenting anaerobes to engender and maintain a local anaerobic environment. Tying up of free oxygen species with iron protoporphyrin IX would also reduce and limit Fe(II)PPIX-mediated oxygen-radical cell damage. More importantly, formation of a cell-surface µ-oxo dimer layer may function as a protective barrier against assault by reactive oxidants generated by neutrophils. Selective interference with these mechanisms would offer the possibility of attenuating the pathogenicity of P. gingivalis and other iron protoporphyrin IX-binding pathogens whose virulence is regulated by this reactive molecule.