Coinvasion of dentinal tubules by Porphyromonas gingivalis and Streptococcus gordonii depends upon binding specificity of streptococcal antigen I/II adhesin

Cell wall-anchored polypeptides of the antigen I/II family are produced by many species of oral streptococci. These proteins mediate adhesion of strep tococci to salivary glycoproteins and to other oral microorganisms and prom ote binding of cells to collagen type I and invasion of dentinal tubules. S ince infections of the root canal system have a mixed anaerobic bacterial e tiology, we investigated the hypothesis that coadhesion of anaerobic bacter ia with streptococci may facilitate invasive endodontic disease. Porphyromo nas gingivalis ATCC 33277 cells were able to invade dentinal tubules when c ocultured with Streptococcus gordonii DL1 (Challis) but not when cocultured with Streptococcus mutans NG8. An isogenic noninvasive mutant of S. gordon ii, with production of SspA and SspB (antigen I/II family) polypeptides abr ogated, was deficient in binding to collagen and had a 40% reduced ability to support adhesion of P. gingivalis. Heterologous expression of the S. mut ans SpaP (antigen I/II) protein in this mutant restored collagen binding an d tubule invasion but not adhesion to P. gingivalis or the ability to promo te P. gingivalis coinvasion of dentin. An isogenic afimbrial mutant of P. g ingivalis had 50% reduced binding to S. gordonii cells but was unaffected i n the ability to coinvade dentinal tubules with S, gordonii wild-type cells . Expression of the S. gordonii SspA or SspB polypeptide on the surface of Lactococcus lactis cells endowed these bacteria with the abilities to bind P. gingivalis, penetrate dentinal tubules, and promote P. gingivalis coinva sion of dentin, The results demonstrate that collagen-binding and P. gingiv alis-binding properties of antigen VII polypeptides are discrete functions. Specificity of antigen VII polypeptide recognition accounts for the abilit y of P. gingivalis to coinvade dentinal tubules with S. gordonii but not wi th S. mutans. This provides evidence that the specificity of interbacterial coadhesion may influence directly the etiology of pulpal and periapical di seases.