Pathogenic factors of Filifactor alocis and Streptococcus gordonii identified in patients with inflammatory periodontal diseases
https://doi.org/10.33925/1683-3759-2025-1092
Abstract
Relevance. One of the key research areas in periodontology is the investigation of the pathogenetic role of individual periodontal pathogens and their microbial associations. With the advent of sequencing technologies and metagenomic analysis, the list of periodontal pathogens continues to expand, and new key pathogens, such as Filifactor alocis, are being identified. Analyzing the virulence factors and interactions of F. alocis with other biofilm-forming bacteria, especially early colonizers such as Streptococcus gordonii, remains an important task.
Objective. The aim of this study was to characterize the pathogenic factors of Streptococcus gordonii and Filifactor alocis in the oral microbiomes of patients with inflammatory periodontal diseases.
Materials and methods. The study involved samples of gingival sulcus contents from healthy individuals (n = 25) and patients with gingivitis (n = 15), as well as samples of periodontal pocket contents from patients with mild (n = 30) and moderate (n = 39) chronic periodontitis (CP). Based on 16S rRNA gene sequencing, the microbial composition of each sample was determined. DNA extracted from the samples was also used as a template for polymerase chain reaction (PCR) to amplify the GspB gene (encoding a serine-rich repeat glycoprotein) and the hsa gene (encoding a sialic acid-binding adhesin) of Streptococcus gordonii, as well as the FtxA gene (encoding an RTX toxin protein) of Filifactor alocis, using primers selected by the authors. Statistical analysis was performed using Statistica 10 software. Cramér’s V coefficient was applied to assess associations between bacterial species occurrence within the oral microbiomes and patient group classification.
Results. 16S rRNA gene sequencing identified Filifactor alocis and Streptococcus gordonii in the microbiomes of patients; these microorganisms were not detected in the microbiomes of healthy individuals. PCR analysis showed that in patients with gingivitis, only the GspB gene was detected (in 6.7% of cases). In patients with mild and moderate chronic periodontitis, both S. gordonii genes (hsa and GspB) were detected in 20% and 28.2% of cases, respectively, and the F. alocis FtxA gene was found in 13.3% and 23.1% of cases, respectively. However, none of the groups exhibited all three genes simultaneously.
Conclusion. S. gordonii and F. alocis are part of the oral microbiota associated with inflammatory periodontal diseases. Identifying their pathogenic factors helps elucidate the mechanisms by which these microorganisms contribute to the onset and progression of periodontal pathology. This knowledge may facilitate the development of more accurate and sensitive early diagnostic tools and support the identification of new therapeutic targets.
Keywords
About the Authors
I. A. GimranovaRussian Federation
Irina A. Gimranova, MD, PhD, Docent, Head of the Department of the Fundamental and Applied Microbiology
3, Lenina str., Ufa, Russian Federation, 450008
A. H. Baymiev
Russian Federation
Andrey H. Baymiev, PhD, DSc, Professor, Department of the Fundamental and Applied Microbiology; Leading Researcher, Laboratory of Plant and Microorganism Bioengineering
Ufa
G. M. Akmalova
Russian Federation
Guzel M. Akmalova, DMD, PhD, DSc, Professor, Department of the Pediatric Dentistry and Orthodontics, Dean
Ufa
V. A. Gritsenko
Russian Federation
Victor A. Gritsenko, MD, PhD, DSc, Professor, Chief Researcher
Orenburg
References
1. Mendes L, Azevedo NF, Felino A, Pinto MG. Relationship between invasion of the periodontium by periodontal pathogens and periodontal disease: a systematic review. Virulence. 2015;6(3):208-215. doi: 10.4161/21505594.2014.984566
2. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, et. al. Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol. 2018; 89(1): 173-S182. doi: 10.1002/JPER.17-0721
3. Imran NK, Abdulbaqi HR, Milward M. The prevalence of periodontitis in an Iraqi population using the 2017 classification. Journal of Baghdad College of Dentistry. 2024;36(2):1-10. doi: 10.26477/jbcd.v36i2.3
4. Abdulbaqi HR, Abdulkareem AA, Alshami ML, Milward MR. The oral health and periodontal diseases awareness and knowledge in the Iraqi population: Online-based survey. Clin Exp Dent Res. 2020;6(5):519-528. doi: 10.1002/cre2.304
5. Dentino A, Lee S, Mailhot J, Hefti AF. Principles of periodontology. Periodontol 2000. 2013;61(1):16-53. doi: 10.1111/j.1600-0757.2011.00397.x
6. Mohammed HA, Abdulkareem AA, Zardawi FM, Gul SS. Determination of the accuracy of salivary biomarkers for periodontal diagnosis. Diagnostics. 2022;12(10):2485. doi: 10.3390/diagnostics12102485
7. Sanz M, Beighton D, Curtis MA, Cury JA, Dige I, Dommisch H, Zaura E. Role of microbial biofilms in the maintenance of oral health and in the development of dental caries and periodontal diseases. J Clin Periodontol. 2017; 44 Suppl 18:S5-S11:5-11. doi: 10.1111/jcpe.12682
8. Deo PN, Deshmukh R. Oral microbiome: Unveiling the fundamentals. J Oral Maxillofac Pathol. 2019;23(1):122-128. doi: 10.4103/jomfp.JOMFP_304_18
9. Kim H, Kim S, Jung S. Instruction of microbiome taxonomic profiling based on 16S rRNA sequencing. J Microbiol. 2020;58(3):193-205. doi: 10.1007/s12275-020-9366-2
10. Mark Welch JL, Rossetti BJ, Rieken CW, Dewhirst FE, Borisy GG. Biogeography of a human oral microbiome at the micron scale. Proc Natl Acad Sci U S A. 2016;113(6):E791-E800. doi: 10.1073/pnas.1522149113
11. Darveau RP. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol. 2010;8(7):481-490. doi: 10.1038/nrmicro2337
12. Evdokimova OV, Kotelevets EP, Novak AI, Biryukov VV. The role of virulence factors of Porphyromonas gingivalis and Tannerella forsythia in the pathogenesis of periodontal diseases: literature review. Clinical Dentistry (Russia). 2025;28(1):171-178 (In Russ.). doi: 10.37988/1811-153X_2025_1_171.
13. Luo A, Wang F, Sun D, Liu X, Xin B. Formation, Development, and Cross-Species Interactions in Biofilms. Front Microbiol. 2022;12:757327. doi: 10.3389/fmicb.2021.757327
14. Kim A, Ahn KB, Kim HY, Seo HS, Yun CH, Han SH. Serine-rich Repeat Adhesin Gordonii Surface Protein B is Important for Streptococcus gordonii Biofilm Formation. Basic Res. 2016;42(12):1767-1772. doi: 10.1016/j.joen.2016.08.016
15. Park OJ, Kwon Y, Park C, So YJ, Park TH, Jeong S, Im J, Yun CH, Han SH. Streptococcus gordonii: Pathogenesis and Host Response to Its Cell Wall Components. Microorganisms. 2020;8(12):1852. doi: 10.3390/microorganisms8121852
16. Nobbs AH, Zhang Y, Khammanivong A, Herzberg MC. Streptococcus gordonii Hsa environmentally constrains competitive binding by Streptococcus sanguinis to saliva-coated hydroxyapatite. J Bacteriol. 2007;189(8):3106-3114. doi: 10.1128/JB.01535-06
17. Wang Q, Wright CJ, Dingming H, Uriarte SM, Lamont RJ. Oral community interactions of Filifactor alocis in vitro. PLoS One. 2013; 8(10): e76271. doi: 10.1371/journal.pone.0076271
18. Chen Y, Bensing BA, Seepersaud R, Mi W, Liao M, Jeffrey PD et. al. Unraveling the sequence of cytosolic reactions in the export of GspB adhesin from Streptococcus gordonii. J Biol Chem. 2018;293(14):5360-5373. doi: 10.1074/jbc.RA117.001284
19. Bensing BA, López JA, Sullam PM. The Streptococcus gordonii Surface Proteins GspB and Hsa Mediate Binding to Sialylated Carbohydrate Epitopes on the Platelet Membrane Glycoprotein Ibα. Infect Immun. 2004;72(11):6528-6537. doi: 10.1128/IAI.72.11.6528-6537.2004
20. Razooqi Z, Khzam N, L'Hostis M, Belibasakis GN, Johansson A, Oscarsson J. Prevalence of the oral pathogen Filifactor alocis and its FtxA toxin related to clinical parameters and presence of Aggregatibacter actinomycetemcomitans. Front Cell Infect Microbiol. 2025;14:1501028. doi: 10.3389/fcimb.2024.1501028
21. Balmasova IP, Tsarev VN, Arutyunov SD, Babaev EA. Filifactor alocis and its role in the etiology of chronic periodontitis. Stomatologiya. 2020;99(3):78-82 (In Russ.). doi: 10.17116/stomat20209903178
22. Oscarsson J, Claesson R, Bao K, Brundin M, Belibasakis GN. Phylogenetic analysis of Filifactor alocis strains isolated from several oral infections identified a novel RTX toxin, ftxA. Toxins. 2020;12(11):687. doi: 10.3390/toxins12110687
23. Ozuna H, Snider I, Belibasakis GN, Oscarsson J, Johansson A, Uriarte SM. Aggregatibacter actinomycetemcomitans and Filifactor alocis: Two exotoxin-producing oral pathogens. Front Oral Health. 2022;3: 981343. doi: 10.3389/froh.2022.981343
24. Razooqi Z, Tjellström I, Höglund Åberg C, Kwamin F, Claesson R, Haubek D, et. al. Association of Filifactor alocis and its RTX toxin gene ftxA with periodontal attachment loss, and in synergy with Aggregatibacter actinomycetemcomitans. Front Cell Infect Microbiol. 2024;14:1501028. doi: 10.3389/fcimb.2024.1501028
25. Aruni W, Chioma O, Fletcher HM. Filifactor alocis: The Newly Discovered Kid on the Block with Special Talents. J Dent Res. 2014;93(8):725-732. doi: 10.1177/0022034514538283
26. Aruni AW, Mishra A, Dou Y, Chioma O, Hamilton BN, Fletcher HM. Filifactor alocis – a new emerging periodontal pathogen. Microbes Infect. 2015;17(7):517-530. doi: 10.1016/j.micinf.2015.03.011
Supplementary files
Review
For citations:
Gimranova IA, Baymiev AH, Akmalova GM, Gritsenko VA. Pathogenic factors of Filifactor alocis and Streptococcus gordonii identified in patients with inflammatory periodontal diseases. Parodontologiya. 2025;30(2):161-169. (In Russ.) https://doi.org/10.33925/1683-3759-2025-1092