Tobacco Smoke Augments Porphyromonas gingivalis - Streptococcus gordonii Biofilm Formation

Abstract

Smoking is responsible for the majority of periodontitis cases in the US and smokers are more susceptible than non-smokers to infection by the periodontal pathogen Porphyromonas gingivalis. P. gingivalis colonization of the oral cavity is dependent upon its interaction with other plaque bacteria, including Streptococcus gordonii. Microarray analysis suggested that exposure of P. gingivalis to cigarette smoke extract (CSE) increased the expression of the major fimbrial antigen (FimA), but not the minor fimbrial antigen (Mfa1). Therefore, we hypothesized that CSE promotes P. gingivalis-S. gordonii biofilm formation in a FimA-dependent manner. FimA total protein and cell surface expression were increased upon exposure to CSE whereas Mfa1 was unaffected. CSE exposure did not induce P. gingivalis auto-aggregation but did promote dual species biofilm formation, monitored by microcolony numbers and depth (both, p<0.05). Interestingly, P. gingivalis biofilms grown in the presence of CSE exhibited a lower pro-inflammatory capacity (TNF-α, IL-6) than control biofilms (both, p<0.01). CSE-exposed P. gingivalis bound more strongly to immobilized rGAPDH, the cognate FimA ligand on S. gordonii, than control biofilms (p<0.001) and did so in a dose-dependent manner. Nevertheless, a peptide representing the Mfa1 binding site on S. gordonii, SspB, completely inhibited dual species biofilm formation. Thus, CSE likely augments P. gingivalis biofilm formation by increasing FimA avidity which, in turn, supports initial interspecies interactions and promotes subsequent high affinity Mfa1-SspB interactions driving biofilm growth. CSE induction of P. gingivalis biofilms of limited pro-inflammatory potential may explain the increased persistence of this pathogen in smokers. These findings may also be relevant to other biofilm-induced infectious diseases and conditions.

Cigarette Smoke Extract–Exposed Methicillin-Resistant Staphylococcus aureus Regulates Leukocyte Function for Pulmonary Persistence

“…CS exposure will, in turn, promote the emergence of hypervirulent strains of staphylococci. In this regard, others and we have shown that CS exposure induces biofilm formation in the respiratory bacterial pathogens S. aureus, Streptococcus pneumoniae, Pseudomonas aeruginosa, and oral pathogens, such as Porphyromonas ginigivalis (11,(30)(31)(32). We previously showed that, at the molecular level, the reactive oxygen species found in CS downregulate the expression of a quorumsensing regulon, agr, while inducing genes encoding a variety of surface proteins involved in biofilm formation and host cell adherence (11).…”

Porphyromonas gingivalis infection in gestational diabetes mellitus and survival in tobacco smokers.

“…Apart from the genes involved in metabolic processes, several genes involved in P. gingivalis attachment to host tissues and other bacterial species were also identified in GAM-CSE model. The genes identified so far are from several studies that have shown increased homotypic and heterotypic biofilm formation by P. gingivalis under the influence of cigarette smoke [157,197,360]. These findings support the idea of increased periodontal pathogen infection in smokers as a result of the dysbiotic influence of P.…”

“…It is considered to be the single major preventable environmental risk factor for chronic periodontitis through its influence on the microbial composition of the biofilm [28,62,157,158] and the host immune system [155].…”

Neutrophils alter epithelial response to Porphyromonas gingivalis in a gingival crevice model.

“…Mechanistically, it is known that smoke exposure alters the activity of multiple P. gingivalis genes and the expression levels of several membrane proteins that result in a lower inflammatory potential of this key pathogen (Bagaitkar et al, 2009(Bagaitkar et al, , 2010(Bagaitkar et al, , 2011.…”