Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates

Abstract

Porphyromonas gingivalis is an aggressive periodontal pathogen that persists in the mixed-species plaque biofilm on tooth surfaces. P. gingivalis cells attach to the plaque commensal Streptococcus gordonii and this coadhesion event leads to the development of P. gingivalis biofilms. Binding of these organisms is multimodal, involving both the P. gingivalis major fimbrial FimA protein and the species-specific interaction of the minor fimbrial Mfa1 protein with the streptococcal SspB protein. This study examined the contribution of the Mfa1-SspB interaction to P. gingivalis biofilm formation. P. gingivalis biofilms readily formed on substrata of S. gordonii DL1 but not on Streptococcus mutans cells which lack a coadhesion-mediating homologue of SspB. An insertional inactivation of the mfa1 gene in P. gingivalis resulted in a phenotype deficient in S. gordonii binding and unable to form biofilms. Furthermore, analysis using recombinant streptococci and enterococci showed that P. gingivalis biofilms formed on Enterococcus faecalis strains expressing SspB or translational fusions of SspB with SpaP (the non-adherent SspB homologue in S. mutans) containing the P. gingivalis adherence domain (SspB adherence region, BAR) of SspB. In contrast, an isogenic Ssp null mutant of S. gordonii DL1 was unable to support biofilm growth, even though this strain bound to P. gingivalis FimA at levels similar to wild-type S. gordonii DL1. Finally, site-specific mutation of two functional amino acid residues in BAR resulted in SspB polypeptides that did not promote the development of P. gingivalis biofilms. These results suggest that the induction of P. gingivalis biofilms on a streptococcal substrate requires functional SspB-minor fimbriae interactions.

Structural and Functional Analysis of Cell Wall-anchored Polypeptide Adhesin BspA in Streptococcus agalactiae

“…Fluid-phase gp340, in saliva and other mucosal secretions, agglutinates microbes for clearance from the body, whereas solid-phase gp340 adsorbed onto host surfaces provides a substratum for microbial adherence (18). AgI/II family polypeptides have also been shown to promote microbial community development by binding to oral bacteria Actinomyces oris (19 -21) or Porphyromonas gingivalis (22,23), as well as to the pathogenic fungus Candida albicans (24). More recently, an AgI/II family polypeptide (group A Streptococcus surface protein, AspA) has been described in group A Streptococcus (GAS) (25).…”

Porphyromonas gingivalis Minor Fimbriae Are Required for Cell-Cell Interactions

“…Although the role of minor fimbriae in P. gingivalis virulence is less well understood, Hiramine et al (6) have shown that the 67-kDa fimbrial protein induces IL-1␣, IL-1␤, and tumor necrosis factor alpha expression in mouse peritoneal macrophages, suggesting their possible involvement in the inflammatory response during the development of periodontal disease. Recent research has shown that minor fimbriae are necessary for the development of P. gingivalis biofilms on streptococcal substrates (7). Coadhesion of P. gingivalis-Streptococcus gordonii requires specific recognition between the 67-kDa and SspB proteins.…”

Novel Model for Multispecies Biofilms That Uses Rigid Gas-Permeable Lenses

“…These intergeneric coadhesion events have been implicated in various aspects of the formation of complex oral microbial biofilms, including the structure, nutritional symbiosis, interspecies communication, and sharing of genetic material (25,26,38,40,41). It is clear from the literature that a number of the species that were employed in developing these biofilms have the potential to coaggregate; however, there are no direct data for some of the strains that were used (5,15,26,28). One study by Foster and Kolenbrander (15) suggested that with Veillonella atypica and A. naeslundii, coaggregation in the planktonic phase affected biofilm formation.…”