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Microorganisms
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Interaction between Oral Microbiota and Immunity in Health and Diseases
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Interaction between Oral Microbiota and Immunity in Health and Diseases

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Medical Microbiology".

Deadline for manuscript submissions: closed (31 May 2023) | Viewed by 16858

Special Issue Editors

Dr. Josefine Hirschfeld

E-Mail Website
Guest Editor
The School of Dentistry, University of Birmingham, Birmingham, United Kingdom
Interests: periodontology; oral immunology and oral microbiology
Dr. Sarah A. Kuehne

E-Mail Website
Guest Editor
The School of Dentistry, University of Birmingham, Birmingham, United Kingdom
Interests: oral microbiology; discovery and characterization of bacterial virulence factors

Special Issue Information

Dear colleagues,

The oral microbiota is composed of biofilms, complex multicellular structures containing microorganisms embedded within a self-produced extracellular matrix, with the ability of interspecies communication. Biofilms are the causative agents of oral diseases like gingivitis, periodontitis, and caries. Specific Gram-negative bacteria, such as Fusobacterium nucleatum, Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans, have been identified over the past decades as pathogens in periodontitis, whereas Gram-positive bacteria, particularly Streptococci, are known to initiate biofilm formation and to cause carious lesions. Gaining a better understanding of the pathogenic potential of microorganisms has been a key area of oral and dental research with the aim to develop novel antimicrobial therapies and early detection methods.

Effector cells of innate and acquired immunity, as well as stromal cells with immune functions, maintain homeostasis in healthy oral conditions but can contribute to disease and mediate host tissue destruction in periodontitis. This collateral damage and the communication between host cells during antimicrobial defense have been another research focus identifying new targets for the prevention and treatment of oral diseases. 

This Special Issue includes the latest research in the field of host-microbiota interactions and microbial communication in oral health and disease, providing further insight into pathobiological mechanisms and highlighting possible diagnostic and therapeutic approaches. 

Dr. Josefine Hirschfeld
Dr. Sarah A. Kuehne
Guest Editors

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Keywords

  • biofilms
  • virulence
  • mucosal immunity
  • host-pathogen interactions
  • homeostasis
  • periodontal diseases

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Published Papers (7 papers)

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Research

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13 pages, 1380 KiB  
Article
The Immune System Response to Porphyromonas gingivalis in Neurological Diseases
by Raffaella Franciotti, Pamela Pignatelli, Domenica Lucia D’Antonio, Rosa Mancinelli, Stefania Fulle, Matteo Alessandro De Rosa, Valentina Puca, Adriano Piattelli, Astrid Maria Thomas, Marco Onofrj, Stefano Luca Sensi and Maria Cristina Curia
Microorganisms 2023, 11(10), 2555; https://doi.org/10.3390/microorganisms11102555 - 13 Oct 2023
Cited by 2 | Viewed by 1442
Abstract
Previous studies have reported an association between oral microbial dysbiosis and the development and progression of pathologies in the central nervous system. Porphyromonas gingivalis (Pg), the keystone pathogen of the oral cavity, can induce a systemic antibody response measured in patients’ [...] Read more.
Previous studies have reported an association between oral microbial dysbiosis and the development and progression of pathologies in the central nervous system. Porphyromonas gingivalis (Pg), the keystone pathogen of the oral cavity, can induce a systemic antibody response measured in patients’ sera using enzyme-linked immunosorbent assays. The present case–control study quantified the immune system’s response to Pg abundance in the oral cavities of patients affected by different central nervous system pathologies. The study cohort included 87 participants: 23 healthy controls (HC), 17 patients with an acute neurological condition (N-AC), 19 patients with a chronic neurological condition (N-CH), and 28 patients with neurodegenerative disease (N-DEG). The results showed that the Pg abundance in the oral cavity was higher in the N-DEG patients than in the HC (p = 0.0001) and N-AC patients (p = 0.01). In addition, the Pg abundance was higher in the N-CH patients than the HCs (p = 0.005). Only the N-CH patients had more serum anti-Pg antibodies than the HC (p = 0.012). The inadequate response of the immune system of the N-DEG group in producing anti-Pg antibodies was also clearly indicated by an analysis of the ratio between the anti-Pg antibodies quantity and the Pg abundance. Indeed, this ratio was significantly lower between the N-DEG group than all other groups (p = 0.0001, p = 0.002, and p = 0.03 for HC, N-AC, and N-CH, respectively). The immune system’s response to Pg abundance in the oral cavity showed a stepwise model: the response diminished progressively from the patients affected with an acute condition to the patients suffering from chronic nervous system disorders and finally to the patients affected by neurodegenerative diseases. Full article
(This article belongs to the Special Issue Interaction between Oral Microbiota and Immunity in Health and Diseases)
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10 pages, 1321 KiB  
Communication
Age-Related Subgingival Colonization of Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis and Parvimonas micra—A Pragmatic Microbiological Retrospective Report
by Rolf Claesson, Anders Johansson and Georgios N. Belibasakis
Microorganisms 2023, 11(6), 1434; https://doi.org/10.3390/microorganisms11061434 - 29 May 2023
Cited by 2 | Viewed by 1391
Abstract
The aim of this study was to compare data about the prevalence and proportions of the bacterial species Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, and Parvimonas micra in periodontitis pocket samples collected from young, <35 years, and old, >35-year-old patients, YP and OP, [...] Read more.
The aim of this study was to compare data about the prevalence and proportions of the bacterial species Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, and Parvimonas micra in periodontitis pocket samples collected from young, <35 years, and old, >35-year-old patients, YP and OP, respectively. The results from the analyses of a total of 3447 subgingival plaque samples analyzed for clinical diagnosis purposes by cultivation regarding the proportions of these species were collected from a database and elucidated. The prevalence of A. actinomycetemcomitans was found to be more than twice as high (OR = 2.96, 95% CI; 2.50–3.50) in samples from the younger (42.2%) than the older group (20.4%) (p < 0.001). The prevalence of P. micra was significantly lower in samples from the younger age group (OR = 0.43, 95%) (p < 0.001), whereas P. gingivalis was similarly distributed (OR = 0.78, 95%) in the two age groups (p = 0.006). A similar pattern was noticed for A. actinomycetemcomitans and P. gingivalis when high proportions (>50%) of the samples of these bacterial species were elucidated. In contrast, the proportion of samples containing >50% with P. micra was lower compared with the two other bacterial species. Furthermore, it was noted that the proportion of samples from old patients containing A. actinomycetemcomitans in combination with P. micra was almost three times higher than in samples when P. micra was replaced by P. gingivalis. In conclusion, A.actinomycetemcomitans showed an increased presence and proportion in samples from young patients compared with the old patients, while P. gingivalis was similarly distributed in the two age groups. P. micra showed an increased presence and proportion in samples from old patients compared with the young patients. Full article
(This article belongs to the Special Issue Interaction between Oral Microbiota and Immunity in Health and Diseases)
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13 pages, 2617 KiB  
Article
Persister Cell Formation and Elevated lsrA and lsrC Gene Expression upon Hydrogen Peroxide Exposure in a Periodontal Pathogen Aggregatibacter actinomycetemcomitans
by Yohei Nakamura, Koji Watanabe, Yoshie Yoshioka, Wataru Ariyoshi and Ryota Yamasaki
Microorganisms 2023, 11(6), 1402; https://doi.org/10.3390/microorganisms11061402 - 26 May 2023
Cited by 3 | Viewed by 2869
Abstract
The effect of hydrogen peroxide, an antiseptic dental treatment, on Aggregatibacter actinomycetemcomitans, the main causative agent of localized invasive periodontitis, was investigated. Hydrogen peroxide treatment (0.06%, 4× minimum inhibitory concentration) resulted in the persistence and survival of approximately 0.5% of the bacterial [...] Read more.
The effect of hydrogen peroxide, an antiseptic dental treatment, on Aggregatibacter actinomycetemcomitans, the main causative agent of localized invasive periodontitis, was investigated. Hydrogen peroxide treatment (0.06%, 4× minimum inhibitory concentration) resulted in the persistence and survival of approximately 0.5% of the bacterial population. The surviving bacteria did not genetically acquire hydrogen peroxide resistance but exhibited a known persister behavior. Sterilization with mitomycin C significantly reduced the number of A. actinomycetemcomitans persister survivors. RNA sequencing of hydrogen peroxide-treated A. actinomycetemcomitans showed elevated expression of Lsr family members, suggesting a strong involvement of autoinducer uptake. In this study, we found a risk of A. actinomycetemcomitans persister residual from hydrogen peroxide treatment and hypothesized associated genetic mechanisms of persister from RNA sequencing. Full article
(This article belongs to the Special Issue Interaction between Oral Microbiota and Immunity in Health and Diseases)
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13 pages, 598 KiB  
Article
Oral Microbiota in Children and Adolescents with Type 1 Diabetes Mellitus: Novel Insights into the Pathogenesis of Dental and Periodontal Disease
by Maria Carelli, Alice Maguolo, Chiara Zusi, Francesca Olivieri, Federica Emiliani, Gelinda De Grandi, Ilaria Unali, Nicoletta Zerman, Caterina Signoretto and Claudio Maffeis
Microorganisms 2023, 11(3), 668; https://doi.org/10.3390/microorganisms11030668 - 6 Mar 2023
Cited by 11 | Viewed by 3122
Abstract
The oral microbiota can be influenced by multiple factors, but only a few studies have focused on the role of glycemic control in determining early alterations of oral microbiota and their association with pathogenesis of both periodontitis and caries. The aim of this [...] Read more.
The oral microbiota can be influenced by multiple factors, but only a few studies have focused on the role of glycemic control in determining early alterations of oral microbiota and their association with pathogenesis of both periodontitis and caries. The aim of this study is to evaluate the interplay between bacteria composition, oral hygiene, and glycemic control in a cohort of children with T1D. A total of 89 T1D children were enrolled (62% males, mean age: 12.6 ± 2.2 years). Physical and clinical characteristics, glucometabolic parameters, insulin treatment, and oral hygiene habits data were collected. Microbiological analysis was performed from saliva samples. A high prevalence of cariogenic and periodontopathogens bacteria in our cohort was detected. In particular, in all subjects Actinomyces spp., Aggregatibacter actinomycetemcomitans, Prevotella intermedia, and Lactobacillus spp. were isolated. S. mutans was found in about half of the analyzed sample (49.4%), in particular in patients with imbalance values of glycemic control. Moreover, a higher presence of both S. mutans and Veillonella spp. was detected in subjects with poorer glycemic control, in terms of HbA1c, %TIR and %TAR, even adjusting for age, sex, and hygiene habits as covariates. Virtuous oral hygiene habits, such as frequency of toothbrush changes and professional oral hygiene, negatively correlated with the simultaneous presence of Tannerella forsythia, Treponema denticola, and Porphyromonas gingivalis, red complex bacteria. Our study shows it is crucial to pay attention to glycemic control and regular oral hygiene to prevent the establishment of an oral microbiota predisposing to dental and periodontal pathology in subjects with T1D since childhood. Full article
(This article belongs to the Special Issue Interaction between Oral Microbiota and Immunity in Health and Diseases)
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20 pages, 8351 KiB  
Article
Dysregulation of Stress-Induced Translational Control by Porphyromonas gingivalis in Host Cells
by Alex A. Knowles, Susan G. Campbell, Neil A. Cross and Prachi Stafford
Microorganisms 2023, 11(3), 606; https://doi.org/10.3390/microorganisms11030606 - 27 Feb 2023
Cited by 2 | Viewed by 2331
Abstract
Porphyromonas gingivalis contributes to the chronic oral disease periodontitis, triggering the activation of host inflammatory responses, inducing cellular stresses such as oxidation. During stress, host cells can activate the Integrated Stress Response (ISR), a pathway which determines cellular fate, by either downregulating protein [...] Read more.
Porphyromonas gingivalis contributes to the chronic oral disease periodontitis, triggering the activation of host inflammatory responses, inducing cellular stresses such as oxidation. During stress, host cells can activate the Integrated Stress Response (ISR), a pathway which determines cellular fate, by either downregulating protein synthesis and initiating a stress–response gene expression program, or by initiating programmed cell death. Recent studies have implicated the ISR within both host antimicrobial defenses and the pathomechanism of certain microbes. In this study, using a combination of immunofluorescence confocal microscopy and immunoblotting, the molecular mechanisms by which P. gingivalis infection alters translation attenuation during oxidative stress-induced activation of the ISR in oral epithelial cells were investigated. P. gingivalis infection alone did not result in ISR activation. In contrast, infection coupled with stress caused differential stress granule formation and composition. Infection heightened stress-induced translational repression independently of core ISR mediators. Heightened translational repression during stress was observed with both P. gingivalis–conditioned media and outer membrane vesicles, implicating a secretory factor in this exacerbated translational repression. The effects of gingipain inhibitors and gingipain-deficient P. gingivalis mutants confirmed these pathogen-specific proteases as the effector of exacerbated translational repression. Gingipains are known to degrade the mammalian target of rapamycin (mTOR) and the findings of this study implicate the gingipain-mTOR axis as the effector of host translational dysregulation during stress. Full article
(This article belongs to the Special Issue Interaction between Oral Microbiota and Immunity in Health and Diseases)
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9 pages, 1597 KiB  
Communication
Aggregatibacter actinomycetemcomitans and Filifactor alocis as Associated with Periodontal Attachment Loss in a Cohort of Ghanaian Adolescents
by Zeinab Razooqi, Carola Höglund Åberg, Francis Kwamin, Rolf Claesson, Dorte Haubek, Jan Oscarsson and Anders Johansson
Microorganisms 2022, 10(12), 2511; https://doi.org/10.3390/microorganisms10122511 - 19 Dec 2022
Cited by 6 | Viewed by 1873
Abstract
The aims of the present study were to document the presence of Aggregatibacter actinomyctemcomitans and the emerging oral pathogen Filifactor alocis, as well as to identify genotypes of these bacterial species with enhanced virulence. In addition, these data were analyzed in relation [...] Read more.
The aims of the present study were to document the presence of Aggregatibacter actinomyctemcomitans and the emerging oral pathogen Filifactor alocis, as well as to identify genotypes of these bacterial species with enhanced virulence. In addition, these data were analyzed in relation to periodontal pocket depth (PPD) and the progression of PPD from the sampled periodontal sites during a two-year period. Subgingival plaque samples were collected from 172 periodontal pockets of 68 Ghanaian adolescents. PPD at sampling varied from 3–14 mm and the progression from baseline, i.e., two years earlier up to 8 mm. The levels of A. actinomycetemcomitans and F. alocis were determined with quantitative PCR. The highly leukotoxic JP2-genotype of A. actinomycetemcomitans and the ftxA a gene of F. alocis, encoding a putative Repeats-in-Toxin (RTX) protein, were detected with conventional PCR. The prevalence of A. actinomycetemcomitans was 57%, and 14% of the samples contained the JP2 genotype. F. alocis was detected in 92% of the samples and the ftxA gene in 52%. The levels of these bacterial species were significantly associated with enhanced PPD and progression, with a more pronounced impact in sites positive for the JP2 genotype or the ftxA gene. Taken together, the results indicate that the presence of both A. actinomycetemcomitans and F. alocis with their RTX proteins are linked to increased PPD and progression of disease. Full article
(This article belongs to the Special Issue Interaction between Oral Microbiota and Immunity in Health and Diseases)
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Review

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11 pages, 990 KiB  
Review
Quorum Sensing in Oral Biofilms: Influence on Host Cells
by Malee Nagi, Iain L. C. Chapple, Praveen Sharma, Sarah A. Kuehne and Josefine Hirschfeld
Microorganisms 2023, 11(7), 1688; https://doi.org/10.3390/microorganisms11071688 - 28 Jun 2023
Cited by 5 | Viewed by 2933
Abstract
Quorum sensing molecules (QSMs) in the oral cavity regulate biofilm formation, the acquisition of iron, stress responses, and the expression of virulence factors. However, knowledge of the direct QSM–host interactions in the oral environment is limited, although their understanding could provide greater insight [...] Read more.
Quorum sensing molecules (QSMs) in the oral cavity regulate biofilm formation, the acquisition of iron, stress responses, and the expression of virulence factors. However, knowledge of the direct QSM–host interactions in the oral environment is limited, although their understanding could provide greater insight into the cross-kingdom communication occurring during oral disease development. This review aims to explore the literature on oral QSM–host interactions and to highlight areas of advancement in this field. The studies included in this review encompass an array of cell types and oral QSMs, with particular emphasis on immune cells and their relationship to periodontal diseases. It can be inferred from the current literature that QSMs are utilised by host cells to detect bacterial presence and, in the majority of cases, elicit an immune response towards the environmental QSMs. This may provide a base to target QSMs as a novel treatment of oral diseases. However, N-acyl homoserine lactone (AHL) detection methods remain an area for development, through which a greater understanding of the influence of oral QSMs on host cells could be achieved. Full article
(This article belongs to the Special Issue Interaction between Oral Microbiota and Immunity in Health and Diseases)
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