Abstract
Periodontal disease depends on the presence of different microorganisms in the oral cavity that during the colonization of periodontal tissues form a multispecies biofilm community, thus allowing them to survive under adverse conditions or facilitate further colonization of host tissues. Not only numerous bacterial species participate in the development of biofilm complex structure but also fungi, especially Candida albicans, that often commensally inhabits the oral cavity. C. albicans employs an extensive armory of various virulence factors supporting its coexistence with bacteria resulting in successful host colonization and propagation of infection. In this article, we highlight various aspects of individual fungal virulence factors that may facilitate the collaboration with the associated bacterial representatives of the early colonizers of the oral cavity, the bridging species, and the late colonizers directly involved in the development of periodontitis, including the “red complex” species. In particular, we discuss the involvement of candidal cell surface proteins—typical fungal adhesins as well as originally cytosolic “moonlighting” proteins that perform a new function on the cell surface and are also present within the biofilm structures. Another group of virulence factors considered includes secreted aspartic proteases (Sap) and other secreted hydrolytic enzymes. The specific structure of the candidal cell wall, dynamically changing during morphological transitions of the fungus that favor the biofilm formation, is equally important and discussed. The non-protein biofilm-composing factors also show dynamic variability upon the contact with bacteria, and their biosynthesis processes could be involved in the stability of mixed biofilms. Biofilm-associated changes in the microbe communication system using different quorum sensing molecules of both fungal and bacterial cells are also emphasized in this review. All discussed virulence factors involved in the formation of mixed biofilm pose new challenges and influence the successful design of new diagnostic methods and the application of appropriate therapies in periodontal diseases.
Highlights
Periodontal disease depends on the presence of different microorganisms in the oral cavity that during the colonization of periodontal tissues form a multispecies biofilm community, allowing them to survive under adverse conditions or facilitate further colonization of host tissues
We highlight various aspects of individual fungal virulence factors that may facilitate the collaboration with the associated bacterial representatives of the early colonizers of the oral cavity, the bridging species, and the late colonizers directly involved in the development of periodontitis, including the “red complex” species
The surface exposed or secreted cysteine proteinases, which activate or degrade complement factors C3 and C5, may lead to the avoidance of complement-mediated detection of accompanying microbiota (Hajishengallis and Lamont, 2012; Hussain et al, 2015). These findings have indicated that the analysis of mixedspecies community formation should be extended to the possible inter-kingdom interactions between bacterial and commensal fungal species belonging to the Candida genus, especially Candida albicans which were found to influence the colonization or metabolic activity of early, bridging, and keystone pathogens of periodontal disease, leading to the onset of severe caries in vivo (Wu et al, 2015; Hwang et al, 2017; Kim et al, 2017; Sztukowska et al, 2018; Bartnicka et al, 2019; Bartnicka et al, 2020)
Summary
Periodontal diseases, belonging to the most common oral diseases worldwide, exert far-reaching consequences for human health, being associated with further systemic diseases such as cardiovascular diseases, diabetes, insulin resistance, gastrointestinal and colorectal cancer, respiratory tract infection, Alzheimer’s disease, and adverse pregnancy outcomes (Kassebaum et al, 2014; Whitmore and Lamont, 2014; Hajishengallis, 2015; Sonti and Fleury, 2015; Vamos et al, 2015; Bui et al, 2019; Liccardo et al, 2019; Dominy et al, 2019; Liu et al, 2021). It was shown that P. gingivalis colonization of a host previously infected with C. albicans caused milder inflammation, leading to prolonged survival of the infected mice, and confirming the chronic nature of the dual-species infection (Bartnicka et al, 2020) For another microorganism highly associated with aggressive periodontal disease, such as Aggregatibacter actinomycetemcomitans, a Gram-negative bacterium belonging to the Aa complex, the ability to inhibit C. albicans filamentation and biofilm formation, mediated by secretory AI-2, was previously demonstrated (Bachtiar et al, 2014; Baker et al, 2017). An increase in the activity of superoxide dismutase (SOD) in the biofilm of soft tissues was noted and according to the study’s authors, this result was associated with an increased presence of anaerobic bacteria (Young et al, 2020)
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