Porphyromonas gingivalis Bundled Fimbriae Interact with Outer Membrane Vesicles, Commensals and Fibroblasts

International Journal of Molecular Sciences, vol. 27, pp. 383

Abstract

Porphyromonas gingivalis plays a key role in periodontal disease and has been associated with several serious systemic diseases. Its fimbriae are a major virulence factor. We recently demonstrated the formation of bundles of long FimA fimbriae in strain ATCC 33277. Transmission (TEM) and scanning electron microscopy (SEM) were used to examine a collection of P. gingivalis strains representing all seven known FimA types (I, Ib, IIa, IIb, III–V) and a P. gulae strain (type A). Additionally, two P. gingivalis strains (ATCC 49417 and OMI 1127) were investigated in dual-species approaches together with Fusobacterium nucleatum or Streptococcus oralis as well as in co-culture with human gingival fibroblasts (HGFs). To evaluate the role of fimbriae accessory proteins FimCDE, proteomic analysis of outer membrane vesicles (OMVs) was performed. Bundling was confirmed to occur regardless of FimA type but was impaired by strong capsule formation. Furthermore, tubular and chain-like outer membrane extensions (OMEs) were identified in most strains examined, including P. gulae. For the first time, fimbriae-associated OMVs (FAVs) were observed. REM images suggest that bundled fimbriae, OMEs and FAVs form connections with F. nucleatum and S. oralis. Proteome analysis of OMV content revealed the ratios of FimA to accessory proteins to be approximately 13:1 for FimC and FimD and approximately 7:1 for FimE. The results imply more accessory proteins per fimbriae or shorter FimA fimbriae in OMVs than in cells. Since FimCDE are known to be responsible for the adhesion properties and autoaggregation of FimA fimbriae, we propose that they could also mediate the stability of bundled fimbriae and the binding of OMVs.

Authors 5

1. Julian Lambertz Aachen Division of Oral Microbiology and Immunology Department of Operative Dentistry

   RWTH Aachen University · Universitätsklinikum Aachen

   Affiliation as printed

   Division of Oral Microbiology and Immunology, Department of Operative Dentistry, Periodontology and Preventive Dentistry, Rheinisch-Westfälische Technische Hochschule (RWTH) University Hospital, 52074 Aachen, Germany

2. Eva Miriam Buhl Aachen Institute of Pathology Electron Microscopy Facility

   RWTH Aachen University · Universitätsklinikum Aachen

   Affiliation as printed

   Electron Microscopy Facility, Institute of Pathology, Rheinisch-Westfälische Technische Hochschule University Hospital, 52074 Aachen, Germany

3. Christian Apel Aachen Institute of Applied Medical Engineering Department of Biohybrid & Medical Textiles (BioTex)

   RWTH Aachen University · Universitätsklinikum Aachen

   Affiliation as printed

   Department of Biohybrid & Medical Textiles (BioTex), Institute of Applied Medical Engineering, Rheinisch-Westfälische Technische Hochschule (RWTH) University Hospital, 52074 Aachen, Germany

4. C Preisinger Aachen Interdisciplinary Center for Clinical Research (IZKF) Proteomics Facility

   RWTH Aachen University · Universitätsklinikum Aachen

   Affiliation as printed

   Proteomics Facility, Interdisciplinary Centre for Clinical Research (IZKF), RWTH Aachen University Hospital, 52074 Aachen, Germany

5. Georg Conrads corresponding Aachen Division of Oral Microbiology and Immunology Department of Operative Dentistry

   RWTH Aachen University · Universitätsklinikum Aachen

   Affiliation as printed

   Division of Oral Microbiology and Immunology, Department of Operative Dentistry, Periodontology and Preventive Dentistry, Rheinisch-Westfälische Technische Hochschule (RWTH) University Hospital, 52074 Aachen, Germany