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Cross-kingdom microbial interactions in dental implant-related infections: is Candida albicans a new villain?

ABSTRACT: Candida albicans, an oral fungal opportunistic pathogen, has shown the ability to colonize implant surfaces and has been frequently isolated from biofilms associated with dental implant-related infections, possibly due to its synergistic interactions with certain oral bacteria. Moreover, evidence suggests that this cross-kingdom interaction on implant can encourage bacterial growth, leading to increased fungal virulence and mucosal damage. However, the role of Candida in implant-related infections has been overlooked and not widely explored or even considered by most microbiological analyses and therapeutic approaches. Thus, we summarized the scientific evidence regarding the ability of C. albicans to colonize implant surfaces, interact in implant-related polymicrobial biofilms, and its possible role in peri-implant infections as far as biologic plausibility. Next, a systematic review of preclinical and clinical studies was conducted to identify the relevance and the gap in the existing literature regarding the role of C. albicans in the pathogenesis of peri-implant infections.

SUBMITTER: Souza JGS

PROVIDER: S-EPMC8933675 | biostudies-literature | 2022 Apr

REPOSITORIES: biostudies-literature

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Cross-kingdom microbial interactions in dental implant-related infections: is Candida albicans a new villain?

Souza João G S JGS Costa Raphael C RC Sampaio Aline A AA Abdo Victória L VL Nagay Bruna E BE Castro Nidia N Retamal-Valdes Belén B Shibli Jamil A JA Feres Magda M Barão Valentim A R VAR Bertolini Martinna M

iScience 20220301 4

<i>Candida albicans</i>, an oral fungal opportunistic pathogen, has shown the ability to colonize implant surfaces and has been frequently isolated from biofilms associated with dental implant-related infections, possibly due to its synergistic interactions with certain oral bacteria. Moreover, evidence suggests that this cross-kingdom interaction on implant can encourage bacterial growth, leading to increased fungal virulence and mucosal damage. However, the role of <i>Candida</i> in implant-re ...[more]

PMID: 35313695

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Project description:Streptococcus mutans and Candida albicans exhibit strong cariogenicity through cross-kingdom biofilm formation during the pathogenesis of dental caries. Caffeic acid phenethyl ester (CAPE), a natural compound, has potential antimicrobial effects on each species individually, but there are no reports of its effect on this dual-species biofilm. This study aimed to explore the effects of CAPE on cariogenic biofilm formation by S. mutans and C. albicans and the related mechanisms. The effect of CAPE on planktonic cell growth was investigated, and crystal violet staining, the anthrone-sulfuric acid assay and confocal laser scanning microscopy were used to evaluate biofilm formation. The structures of the formed biofilms were observed using scanning electron microscopy. To explain the antimicrobial effect of CAPE, quantitative real-time PCR (qRT-PCR) was applied to monitor the relative expression levels of cariogenic genes. Finally, the biocompatibility of CAPE in human oral keratinocytes (HOKs) was evaluated using the CCK-8 assay. The results showed that CAPE suppressed the growth, biofilm formation and extracellular polysaccharides (EPS) synthesis of C. albicans and S. mutans in the coculture system of the two species. The expression of the gtf gene was also suppressed by CAPE. The efficacy of CAPE was concentration dependent, and the compound exhibited acceptable biocompatibility. Our research lays the foundation for further study of the application of the natural compound CAPE as a potential antimicrobial agent to control dental caries-associated cross-kingdom biofilms. IMPORTANCE Severe dental caries is a multimicrobial infectious disease that is strongly induced by the cross-kingdom biofilm formed by S. mutans and C. albicans. This study aimed to investigate the potential of caffeic acid phenethyl ester (CAPE) as a natural product in the prevention of severe caries. This study clarified the inhibitory effect of CAPE on cariogenic biofilm formation and the control of cariogenic genes. It deepens our understanding of the synergistic cariogenic effect of S. mutans and C. albicans and provides a new perspective for the prevention and control of dental caries with CAPE. These findings may contribute to the development of CAPE as a promising antimicrobial agent targeting this caries-related cross-kingdom biofilm.

Project description:Candida albicans is frequently detected with heavy infection by Streptococcus mutans in plaque-biofilms from children with early-childhood caries (ECC). This cross-kingdom biofilm contains an extensive matrix of extracellular α-glucans that is produced by an exoenzyme (GtfB) secreted by S. mutans. Here, we report that mannans located on the outer surface of C. albicans cell-wall mediates GtfB binding, enhancing glucan-matrix production and modulating bacterial-fungal association within biofilms formed in vivo. Using single-molecule atomic force microscopy, we determined that GtfB binds with remarkable affinity to mannans and to the C. albicans surface, forming a highly stable and strong bond (1-2 nN). However, GtfB binding properties to C. albicans was compromised in strains defective in O-mannan (pmt4ΔΔ) or N-mannan outer chain (och1ΔΔ). In particular, the binding strength of GtfB on och1ΔΔ strain was severely disrupted (>3-fold reduction vs. parental strain). In turn, the GtfB amount on the fungal surface was significantly reduced, and the ability of C. albicans mutant strains to develop mixed-species biofilms with S. mutans was impaired. This phenotype was independent of hyphae or established fungal-biofilm regulators (EFG1, BCR1). Notably, the mechanical stability of the defective biofilms was weakened, resulting in near complete biomass removal by shear forces. In addition, these in vitro findings were confirmed in vivo using a rodent biofilm model. Specifically, we observed that C. albicans och1ΔΔ was unable to form cross-kingdom biofilms on the tooth surface of rats co-infected with S. mutans. Likewise, co-infection with S. mutans defective in GtfB was also incapable of forming mixed-species biofilms. Taken together, the data support a mechanism whereby S. mutans-secreted GtfB binds to the mannan layer of C. albicans to promote extracellular matrix formation and their co-existence within biofilms. Enhanced understanding of GtfB-Candida interactions may provide new perspectives for devising effective therapies to disrupt this cross-kingdom relationship associated with an important childhood oral disease.

Dataset Information

Cross-kingdom microbial interactions in dental implant-related infections: is Candida albicans a new villain?

Publications

Cross-kingdom microbial interactions in dental implant-related infections: is Candida albicans a new villain?

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