Porphyromonas gingivalis during Periodontitis Pathogenesis: History
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Contributor:
Josefa Nuñez-Belmar
,
Mauricio Morales-Olavarria
,
Emiliano Vicencio
,
Rolando Vernal
,
Cristian Cortez
,
Juan P. Cárdenas

Periodontitis is a non-communicable chronic inflammatory disease characterized by the progressive and irreversible breakdown of the soft periodontal tissues and resorption of teeth-supporting alveolar bone. The etiology of periodontitis involves dysbiotic shifts in the diversity of microbial communities inhabiting the subgingival crevice, which is dominated by anaerobic Gram-negative bacteria, including Porphyromonas gingivalis. Indeed, P. gingivalis is a keystone pathogen with a repertoire of attributes that allow it to colonize periodontal tissues and influence the metabolism, growth rate, and virulence of other periodontal bacteria. The pathogenic potential of P. gingivalis has been traditionally analyzed using classical biochemical and molecular approaches.

  • periodontitis
  • microbial dysbiosis
  • Porphyromonas gingivalis
  • keystone pathogen

1. Introduction

Periodontitis is a non-communicable chronic inflammatory disease characterized by the progressive and irreversible destruction of the periodontium [1][2]. Periodontitis is a long-term disease with a high prevalence worldwide, being the most prevalent form of osteolytic pathology in humans [3][4]. The etiology of periodontitis lies in the constant challenge of the dysbiotic biofilm attached to the tooth in the subgingival crevice, which leads to a deregulated host immune response responsible for the clinical phenotype of the disease [5].
Porphyromonas gingivalis is a well-characterized member of the dysbiotic subgingival microbiota and a key bacterium in the aetiopathogenesis of periodontitis [6][7]. It is an anaerobe, asaccharolytic, non-motile, Gram-negative bacterium associated with destructive chronic periodontitis [8]. Its association with periodontitis is based fundamentally on its virulence properties, recurrent presence in affected sites, and higher serum antibody levels in patients diagnosed with chronic periodontitis. In addition, periodontal health indicators are inversely correlated with the presence of this periodontal pathogen [8][9][10]. Moreover, periodontitis induced by P. gingivalis may influence the course and pathogenesis of other chronic inflammatory disorders [11]. P. gingivalis expresses several virulence factors that enable it to colonize, invade, and disrupt periodontal tissues [8][12]. Despite its low-relative abundance in the subgingival biofilm, P. gingivalis operates as a keystone pathogen, being critical in promoting the host inflammatory and osteolytic response involved in periodontitis onset and progression [7][13][14]. Furthermore, P. gingivalis significantly changes the bacterial taxa that comprise symbiotic microbial communities for heterotypical communities with recognized destructive inflammatory potential [6][7] (Figure 1). P. gingivalis strain virulence varies among different types, and this diversity may alter its keystone pathogen capacity [14][15][16]. Consequently, precise analysis methods are required for a better understanding of P. gingivalis in the context of its different pathogenic potential and its modulating effect on multispecies heterotopic communities in the periodontitis-related biofilm.
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Figure 1. Periodontitis pathogenesis and P. gingivalis overview. (A) During the onset and progression of periodontitis, P. gingivalis resides in the subgingival biofilm adhered to the tooth surface, where it interacts metabolically with other bacteria, inducing them to express different virulence factors with pathogenic potential. In parallel, P. gingivalis acts as a keystone pathogen, altering the regulation of the immune response in the susceptible host. The metabolic synergism and immune response subversion provide the nutritional and protective conditions required by the dysbiotic subgingival community to increase their diversity and abundance, with the concomitant induction of a strong, destructive inflammatory response. Together, all these activities cause irreversible connective tissue breakdown and resorption of the tooth-supporting alveolar bone, the critical hallmark of periodontitis that causes tooth loss. (B) To invade the periodontium, P. gingivalis uses various virulence factors that allow it to colonize, replicate, and spread in different subsets of cells to increase its progeny and generate infection. (C) In addition to causing tooth loss, P. gingivalis-induced periodontitis can also affect systemic health, influencing the course of other diseases and conditions.
Omics technologies have revolutionized modern biology, enabling simultaneous analysis of multiple molecular components in response to environmental stimuli across time [17]. These technological approaches, mainly metagenomics, metatranscriptomics, proteomics, and metabolomics, have the potential to increase the efficiency of information to elucidate complex systems [18] and have been used to understand the composition and function of the oral microbiome during health and disease [19][20][21].

2. P. gingivalis Is a Keystone Pathogen of Periodontitis

As a keystone pathogen, P. gingivalis disrupts the host’s immune response even at low relative abundances [22][23]. This microbe generates protection and the optimal nutritional conditions for the growth and development of pathobiont microorganisms, responsible for maintaining the destructive chronic inflammatory environment [24]. Therefore, P. gingivalis modulates the entire bacterial community’s composition, abundance, and adaptive fitness [25][26]. This synergistic interaction was evidenced in a mechanistic study using germ-free mice. In contrast to wild-type mice, the oral microbiota lack in germ-free mice did not induce destructive inflammation after P. gingivalis inoculation into the periodontal tissues [13].
The oral microbiome comprises over 600 prevalent taxa distributed in different ecological niches. Because many of these species cannot be cultured, omics technologies are powerful tools for assessing their composition [27]. Using clinical samples, metagenomics and metatranscriptomics studies have confirmed the prominent subgingival microbial dysbiosis in individuals with periodontitis. Furthermore, they established the presence and relative abundance of P. gingivalis and the virulence factors upregulation associated with its pathogenesis [19][28][29][30].
The synergy interactions of the resident microbiota are fundamental in this new periodontitis model. In this sense, Streptococcus gordonii is an accessory pathogen that contributes to increasing P. gingivalis virulence [7]. LuxS is a soluble mediator autoinducer 2 (AI-2) molecule of P. gingivalis involved in the uptake of hemin/inorganic iron and quorum sensing interspecies with Streptococcus gordonii. Utilizing transcriptomics was demonstrated in a LuxS-deficient strain that P. gingivalis fails to form microcolonies, confirming the significance of these molecules in the signaling involved in the formation and maturation of the biofilm [31]. The role of keystone bacteria has also been evaluated in vitro. A multispecies symbiotic biofilm (oral health) was generated in the presence or absence of P. gingivalis and A. actinomycetemcomitans. The transcriptomic analyses showed significant gene expression pattern differences when comparing both conditions. Similarly, they exhibited different gene expressions when planktonic, and biofilm conditions were compared. These findings showed a two-way modulatory effect of periodontal pathogens on multispecies heterotypic communities [32]. The keystone pathogen effect has also been evaluated in in vivo models. The ligature-induced periodontitis model in mice induces microbial dysbiosis and recreates the destructive inflammatory conditions exhibited during periodontitis in humans [33]. Sterile silk ligature alone causes alveolar bone resorption. However, when it is preincubated with P. gingivalis and subsequently tied to the tooth, the concomitant bone loss is significantly exacerbated [34]. Consistent with the systemic effects of periodontitis, oral administration of P. gingivalis significantly alters the gut microbiome. The metagenomic studies showed evident differences in the composition and relative abundance of the community members compared to mice that did not receive P. gingivalis. In addition, dysbiosis generates systemic inflammatory effects, changes in the serum metabolome, and aggravates collagen-induced arthritis [35][36][37][38]. This evidence reveals the contribution of omics disciplines to determining the keystone role of P. gingivalis in perturbing bacterial communities.

3. Proteomics and Metabolomics in P. gingivalis Pathogenesis

Proteomics corresponds to the study (Table 1) of the structure, function, and protein interaction on a large scale [39]. This technique has become a powerful tool for protein identification involved in host-P. gingivalis interactions and their relationship with other oral bacteria. For example, proteomic studies using mixed oral bacteria cultures showed that nearly 40% of P. gingivalis proteins can be regulated by the presence of other members of the oral microbiota, such as Fusobacterium nucleatum, Streptococcus gordonii, or Streptococcus oralis [40][41], suggesting an effect of the ecological community on P. gingivalis protein expression.
Table 1. Summary of metabolomics and proteomics research studies.
Strategy Method and Sample Findings/Contributions Reference
Proteomics Cultured P. gingivalis, F. nucleatum, and S. gordonii mixed biofilm and P. gingivalis monobiofilm as control. Bacterial cells were lysed, and proteins were digested for mass spectrometry. The proteome of the mixed biofilm differs from the monobiofilm, it exhibits a decrease in proteins involved in cell shape and cell envelope formation, and an increase in HmuR protein (an outer membrane receptor). [40]
Proteomics Cultured P. gingivalis (ATCC®33277™) and S. oralis (ATCC®9811™) mixed biofilm. Controls are monobiofilm of P. gingivalis and S. oralis. Biofilm samples were digested and then summited to shotgun proteomic analysis with LC-MS/MS. The P. gingivalis proteins that increased their expression induced by the interaction with S. oralis were GyrB, RpoD, FimA and a probable transcriptional regulatory protein. [41]
Proteomics Liquid cultured P. gingivalis (ATCC®33277™, W83 and two peptidylarginine deiminase (PPAD) mutant strains) were centrifugated and the supernatant was analyzed by mass spectrometry analysis. Analysis of the P. gingivalis proteome and extracellular citrulilnome showed heterogeneity between the different isolates. Furthermore, the main virulence factors revealed different patterns in their citrullination. [42]
Proteomics Cultured P. gingivalis ATCC®33277™ and mutant strains. Cells were harvested, lysed, and the supernatant was subjected to mass spectrometry analysis. Identification of 257 putative O-glycosylation sites within 145 glycoproteins of P. gingivalis. Demonstration for the first time the presence of the O-glycosylation system in P. gingivalis. [43]
Proteomics Cultured P. gingivalis (W50 strain), then cells were harvested and centrifuged, and the supernatant was filtered to obtain outer membrane vesicles (OMVs) for mass spectrometry analysis. A total of 151 OMV proteins were identified and the most enriched proteins were LptO, IhtB and HmuY. [44]
Proteomics Cultured P. gingivalis (W50 strain) in three conditions: control, heme limitation, and heme excess conditions. Then cells were harvested and processed to obtain whole cell lysate and outer membrane vesicles separately and then mass spectrometry analyses. The proteins most upregulated in response to heme limitation were those involved in binding and transporting heme. [45]
Metabolomics Tongue swabs and mouth washout samples from patients with chronic periodontal disease were analyzed with proton nuclear magnetic resonance (H-NMR) to determine their metabolic status. The metabolic state of the mouth of chronic periodontal disease patients changes in the levels of eight metabolites in comparison to healthy individuals. These metabolic changes could be used as a periodontal disease-associated process biomarker. [46]
Metabolomics Meditation through Gas chromatography-mass spectrometer (GC-MS) metabolite profiling of cultured human periodontal ligament fibroblast infected with P. gingivalis (ATCC®33277™). Periodontal ligament cells (PDLSCs) experienced metabolic reprogramming due to the infection of P. gingivalis. These metabolic changes could be related to pro-inflammatory responses on PDLSC, showing a shift from oxidative phosphorylation to glycolysis. [47]
Metabolomics and metagenomics Serum samples from mice submitted to an oral gavage of P. gingivalis (ATCC®33277TM) and sham control were analyzed with Untargeted metabolomics profiling chromatographic separation and mass spectrometry (MS). Additionally, RNA extraction and metagenomic analysis were done in colon samples from the same study groups. The analysis of the metabolites in P. gingivalis-administered mice demonstrated that oral administration of this periodontal pathogen could induce dysbiosis of the gut microbiota. In addition, these derived metabolites are associated with metabolic pathways and could be related to the development of metabolic disorders and the destruction of intestinal barrier function. [48]
The identification and characterization of proteins involved in bacterial colonization and invasion is another relevant scope of P. gingivalis proteomics. Notable changes have been reported in the extracellular proteomic profiles and virulence factors expressed by different strains of P. gingivalis [42]. For instance, using mass spectrometry, alterations in the P. gingivalis O-glycoproteome are evidenced, determining that gingipains lacked these post-translational modifications [43]. On the other hand, a previously known marker of rheumatoid arthritis is the loss of tolerance to the presence of proteins that have undergone citrullination. This post-translational modification affects arginine residues and produces changes in the structure and function of proteins [49]. Interestingly, P. gingivalis contains a peptidyl-arginine deiminase (PPAD), an enzyme capable of protein citrullination, and it can modify bacterial and human proteins [42]. Moreover, the comparison of secreted protein citrullination profiles among several P. gingivalis clinical isolates with reference strains showed substantial differences, primarily focused on six to 25 proteins, mostly composed of virulence factors. The role of these modifications remains to be clarified.
Proteomics can also help to understand the role of some cellular derivates, such as Outer membrane vesicles (OMVs). P. gingivalis releases several virulence factors toward the environment via OMVs [44]. Studies covering the role of OMV-associated proteome in P. gingivalis suggest important changes according to the availability of heme, displaying an upregulation of proteins involved in heme binding and transport when this nutrient is limited [45]. Collectively, proteomic studies reveal that the P. gingivalis proteome changes depending on the interaction target and the biological context, offering another opportunity to understand P. gingivalis physiology and pathogenesis.
Another useful technique to understand the role of P. gingivalis in periodontitis is metabolomics (Table 1), which is the systematic study of metabolic content produced and consumed by specific cellular processes. Thus, it presents the collection of all metabolites within a particular sample [50]. Current evidence suggests that during periodontitis, a metabolic alteration in the oral cavity is induced by the colonization of pathogenic bacteria [48]. Additionally, metabolic changes are also reported in cells of the periodontal ligament (PDLSCs) under P. gingivalis infection, showing a metabolic reprogramming that compromises processes associated with the glycolysis, tricarboxylic acid (TCA) cycle, tryptophan, and choline metabolism [47][48]. Since gene sequence and expression profiles are essential but not sufficient to understand the mechanisms underlying P. gingivalis pathogenesis, proteomic and metabolomic studies have begun to gain more insights into periodontitis-related host-pathogen interactions.

This entry is adapted from the peer-reviewed paper 10.3390/ijms24010620

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