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Cross-Kingdom Cell-to-Cell Interactions in Cariogenic Biofilm Initiation.

ABSTRACT: Candida albicans is known to form polymicrobial biofilms with various Streptococcus spp., including mitis and mutans group streptococci. Streptococcus gordonii (mitis group) has been shown to bind avidly to C. albicans hyphae via direct cell-to-cell interaction, while the cariogenic pathogen Streptococcus mutans (mutans group) interacts with the fungal cells via extracellular glucans. However, the biophysical properties of these cross-kingdom interactions at the single-cell level during the early stage of biofilm formation remain understudied. Here, we examined the binding forces between S. mutans (or S. gordonii) and C. albicans in the presence and absence of in situ glucans on the fungal surface using single-cell atomic force microscopy and their influence on biofilm initiation and subsequent development under cariogenic conditions. The data show that S. gordonii binding force to the C. albicans surface is significantly higher than that ofS. mutans to the fungal surface (~2-fold). However, S. mutans binding forces are dramatically enhanced when the C. albicans cell surface is locally coated with extracellular glucans (~6-fold vs. uncoated C. albicans), which vastly exceeds the forces between S. gordonii andC. albicans. The enhanced binding affinity of S. mutans to glucan-coated C. albicans resulted in a larger structure during early biofilm initiation compared to S. gordonii-C. albicans biofilms. Ultimately, this resulted in S. mutans dominance composition in the 3-species biofilm model under cariogenic conditions. This study provides a novel biophysical aspect of Candida-streptococcal interaction whereby extracellular glucans may selectively favor S. mutans binding interactions with C. albicans during cariogenic biofilm development.

SUBMITTER: Wan SX

PROVIDER: S-EPMC7755950 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Candida albicans, a major opportunistic fungal pathogen is frequently found together with Streptococcus mutans in dental biofilms associated with severe childhood tooth-decay, a prevalent pediatric oral disease. Previous studies have demonstrated that S. mutans and C. albicans synergizes virulence of plaque-biofilms in vivo. However, the nature of this bacterial-fungal relationship in this cross-kingdom biofilm remains largely uncharacterized. Using iTRAQ based quantitative proteomics, we found that proteins associated with carbohydrate metabolism such as alpha-1,4 glucan phosphorylase, Hexokinase-2, Isocitrate lyase and malate synthase were significantly upregulated in C. albicans in the mixed-species biofilms (P<0.05). C. albicans proteins associated with growth/morphogenesis such as pH-responsive protein-2, Fma1p and Hsp21 were also induced. Conversely, S. mutans proteins in the tricarboxylic acid cycle such as citrate synthase and in the pentose phosphate pathway such as Ribose-5-phosphate isomerase A as well as proteins associated with sugar transport systems were upregulated indicating enhanced carbohydrate metabolism. Interestingly mixed-species biofilm microenvironment had a lower pH than S. mutans single-species biofilms. This observation was supported by proteomics, wherein proteins associated with lactate and formate assimilation such as Glyoxalase and putative NADPH-dependent methylglyoxal reductase proteins were significantly upregulated in the mixed-species biofilms (P<0.05). Furthermore, we unexpectedly found that S. mutans derived glucosyltransferase B (GtfB), responsible for co-adhesion via glucans, can also contribute to C. albicans growth and carbohydrate metabolism by providing glucose and fructose from sucrose breakdown. These findings demonstrate synergistic bacterial-fungal interactions within mixed-species biofilms and a novel GtfB cross-feeding role. Taken together, quantitative proteomics provides new insights into this virulent cross-kingdom oral biofilm.

Project description:Dental caries is a biofilm-mediated disease that occurs when acidogenic/aciduric bacteria obtain an ecological advantage over commensal species. In previous studies, the effects of the antimicrobial peptide GH12 on planktonic bacteria and monospecies biofilms were confirmed. The objectives of this study were to investigate the effects of GH12 on a cariogenic multispecies biofilm and to preliminarily explain the mechanism. In this biofilm model, Streptococcus mutans ATCC 70061 was the representative of cariogenic bacteria, while Streptococcus gordonii ATCC 35105 and Streptococcus sanguinis JCM 5708 were selected as healthy microbiota. The results showed that GH12 was more effective in suppressing S. mutans than the other two species, with lower MIC and minimal bactericidal concentration (MBC) values among diverse type strains and clinical isolated strains. Therefore, GH12, at no more than 8 mg/liter, was used to selectively suppress S. mutans in the multispecies biofilm. GH12 at 4 mg/liter and 8 mg/liter reduced the cariogenic properties of the multispecies biofilm in biofilm formation, glucan synthesis, and lactic acid production. In addition, GH12 suppressed S. mutans within the multispecies biofilm and changed the bacterial composition. Furthermore, 8 mg/liter GH12 showed a selective bactericidal impact on S. mutans, and GH12 promoted hydrogen peroxide production in S. sanguinis and S. gordonii, which improved their ecological advantages. In conclusion, GH12 inhibited the cariogenic properties and changed the composition of the multispecies biofilm through a two-part mechanism by which GH12 directly suppressed the growth of S. mutans as well as enhanced the ecological competitiveness of S. sanguinis and S. gordoniiIMPORTANCE Dental caries is one of the most prevalent chronic infectious diseases worldwide, with substantial economic and quality-of-life impacts. Streptococcus mutans has been considered the principal pathogen of dental caries. To combat dental caries, an antimicrobial peptide, GH12, was designed, and its antibacterial effects on planktonic S. mutans and the monospecies biofilm were confirmed. As etiological concepts of dental caries evolved to include microecosystems, the homeostasis between pathogenic and commensal bacteria and a selective action on cariogenic virulence have increasingly become the focus. The novelty of this research was to study the effects of the antimicrobial peptides on a controlled cariogenic multispecies biofilm model. Notably, the role of an antimicrobial agent in regulating interspecific competition and composition shifts within this multispecies biofilm was investigated. With promising antibacterial and antibiofilm properties, the use of GH12 might be of importance in preventing and controlling caries and other dental infections.

Project description:Pregnancy initiates a temporary transition in the maternal physiological state, with a shift in the oral microbiome and a potential increase in frequency of oral diseases. The risk of oral disease is higher among populations of Hispanic and Black women and those with lower socioeconomic status (low SES), demonstrating a need for intervention within these high-risk populations. To further our understanding of the oral microbiome of high-risk pregnant women, we characterized the oral microbiome in 28 nonpregnant and 179 pregnant low-SES women during their third trimester living in Rochester, New York. Unstimulated saliva and supragingival plaque samples were collected cross-sectionally, followed by assessment of the bacterial (16S ribosomal RNA) and fungal (18S ITS) microbiota communities. Trained and calibrated dentists performed oral examinations to determine the number of decayed teeth and plaque index. Initially, plaque from 28 nonpregnant women and 48 pregnant women were compared; these data showed significant differences in bacterial abundances based on pregnancy status. To further our understanding of the oral microbiome within the pregnant population, we next examined the oral microbiome within this population based on several variables. Streptococcus mutans, Streptococcus oralis, and Lactobacillus were associated with a greater number of decayed teeth. The composition of fungal communities differed between plaque and saliva, demonstrating 2 distinct "mycotypes" that were represented by a greater abundance of Candida in plaque and Malassezia in saliva. Veillonella rogosae, a common oral bacterium, was negatively associated with both plaque index and salivary Candida albicans colonization by culture data. This was further emphasized by in vitro inhibition of C. albicans by V. rogosae. Identification of interactions between the bacterial or fungal oral communities revealed that V. rogosae was positively associated with the oral commensal Streptococcus australis and negatively with the cariogenic Lactobacillus genus, suggesting V. rogosae as a potential biomarker of a noncariogenic oral microbiome.

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Cross-Kingdom Cell-to-Cell Interactions in Cariogenic Biofilm Initiation.

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