Potential prebiotic substrates modulate composition, metabolism, virulence and inflammatory potential of an in vitro multi-species oral biofilm.
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ABSTRACT:
SUBMITTER: Verspecht T
PROVIDER: S-EPMC8079042 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Previous research identified potential prebiotic substrates for oral health like the structural analogues N-acetyl-D-mannosamine (NADM) and N-acetyl-D-glucosamine (NADG). The main hypothesis of the current study was twofold. Firstly, it was hypothesized that the modulatory effects of NADM are not limited to changes in multi-species oral biofilm composition, but also include effects on metabolism, virulence, and inflammatory potential. Secondly, the presence and orientation of their N-acetyl group could play a role. Therefore, a comparison was made between the effects of NADM, NADG and D-(+)-mannose on multi-species oral biofilms. Besides a beneficial compositional shift, NADM-treated biofilms also showed an altered metabolism, a reduced virulence and a decreased inflammatory potential. At a substrate concentration of 1 M, these effects were pronounced for all biofilm aspects, whereas at ~ 0.05 M (1%(w/v)) only the effects on virulence were pronounced. When comparing between substrates, both the presence and orientation of the N-acetyl group played a role. However, this was generally only at 1 M and dependent on the biofilm aspect. Overall, NADM was found to have different effects at two concentrations that beneficially modulate in vitro multi-species oral biofilm composition, metabolism, virulence and inflammatory potential. The presence and orientation of the N-acetyl group influenced these effects.
| S-EPMC8298493 | biostudies-literature
Project description:The salivary glands actively concentrate plasma nitrate, leading to high salivary nitrate concentrations (5-8 mM) after a nitrate-rich vegetable meal. Nitrate is an ecological factor that can induce rapid changes in structure and function of polymicrobial communities, but the effects on the oral microbiota have not been clarified. To test this, saliva of 12 healthy donors was collected to grow in vitro biofilms with and without 6.5 mM nitrate. Samples were taken at 5 h (most nitrate reduced) and 9 h (all nitrate reduced) of biofilm formation for ammonium, lactate and pH measurements, as well as 16S rRNA gene Illumina sequencing. Nitrate did not affect biofilm growth significantly, but reduced lactate production, while increasing the observed ammonium production and pH (all p < 0.01). Significantly higher levels of the oral health-associated nitrate-reducing genera Neisseria (3.1 ×) and Rothia (2.9 ×) were detected in the nitrate condition already after 5 h (both p < 0.01), while several caries-associated genera (Streptococcus, Veillonella and Oribacterium) and halitosis- and periodontitis-associated genera (Porphyromonas, Fusobacterium, Leptotrichia, Prevotella, and Alloprevotella) were significantly reduced (p < 0.05 at 5 h and/or 9 h). In conclusion, the addition of nitrate to oral communities led to rapid modulation of microbiome composition and activity that could be beneficial for the host (i.e., increasing eubiosis or decreasing dysbiosis). Nitrate should thus be investigated as a potential prebiotic for oral health.
| S-EPMC7393384 | biostudies-literature
Project description:Recent studies have shown phenotypic and metabolic heterogeneity in related species including Streptococcus oralis, a typical oral commensal bacterium, Streptococcus mutans, a cariogenic bacterium, and Streptococcus gordonii, which functions as an accessory pathogen in periodontopathic biofilm. In this study, metabolites characteristically contained in the saliva of individuals with good oral hygiene were determined, after which the effects of an identified prebiotic candidate, D-tagatose, on phenotype, gene expression, and metabolic profiles of those three key bacterial species were investigated. Examinations of the saliva metabolome of 18 systemically healthy volunteers identified salivary D-tagatose as associated with lower dental biofilm abundance in the oral cavity (Spearman's correlation coefficient; r = -0.603, p = 0.008), then the effects of D-tagatose on oral streptococci were analyzed in vitro. In chemically defined medium (CDM) containing D-tagatose as the sole carbohydrate source, S. mutans and S. gordonii each showed negligible biofilm formation, whereas significant biofilms were formed in cultures of S. oralis. Furthermore, even in the presence of glucose, S. mutans and S. gordonii showed growth suppression and decreases in the final viable cell count in a D-tagatose concentration-dependent manner. In contrast, no inhibitory effects of D-tagatose on the growth of S. oralis were observed. To investigate species-specific inhibition by D-tagatose, the metabolomic profiles of D-tagatose-treated S. mutans, S. gordonii, and S. oralis cells were examined. The intracellular amounts of pyruvate-derived amino acids in S. mutans and S. gordonii, but not in S. oralis, such as branched-chain amino acids and alanine, tended to decrease in the presence of D-tagatose. This phenomenon indicates that D-tagatose inhibits growth of those bacteria by affecting glycolysis and its downstream metabolism. In conclusion, the present study provides evidence that D-tagatose is abundant in saliva of individuals with good oral health. Additionally, experimental results demonstrated that D-tagatose selectively inhibits growth of the oral pathogens S. mutans and S. gordonii. In contrast, the oral commensal S. oralis seemed to be negligibly affected, thus highlighting the potential of administration of D-tagatose as an oral prebiotic for its ability to manipulate the metabolism of those targeted oral streptococci.
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Project description:Streptococcus mutans and Candida albicans are found together in the oral biofilms on dental surfaces, but little is known about the ecological interactions between these species. Here, we studied the effects of S. mutans UA159 on the growth and pathogencity of C. albicans. Initially, the effects of S. mutans on the biofilm formation and morphogenesis of C. albicans were tested in vitro. Next, we investigate the influence of S. mutans on pathogenicity of C. albicans using in vivo host models, in which the experimental candidiasis was induced in G. mellonella larvae and analyzed by survival curves, C. albicans count in hemolymph, and quantification of hyphae in the host tissues. In all the tests, we evaluated the direct effects of S. mutans cells, as well as the indirect effects of the subproducts secreted by this microorganism using a bacterial culture filtrate. The in vitro analysis showed that S. mutans cells favored biofilm formation by C. albicans. However, a reduction in biofilm viable cells and inhibition of hyphal growth was observed when C. albicans was in contact with the S. mutans culture filtrate. In the in vivo study, injection of S. mutans cells or S. mutans culture filtrate into G. mellonella larvae infected with C. albicans increased the survival of these animals. Furthermore, a reduction in hyphal formation was observed in larval tissues when C. albicans was associated with S. mutans culture filtrate. These findings suggest that S. mutans can secrete subproducts capable to inhibit the biofilm formation, morphogenesis and pathogenicity of C. albicans, attenuating the experimental candidiasis in G. mellonella model.
| S-EPMC4774980 | biostudies-literature
Project description:In this work, we want to investigate the impact of different substrates and different environmental condition on the biofilm communities growing on plaster, marble, and mortar substrates inside the Herculaneum Suburban Baths. To do so, we measured environmental conditions and sampled biofilm communities along the walls of the baths and used culture-dependent and -independent molecular techniques (DGGE) to identify the species at each sampling sites. We used the species pool to infer structure and richness of communities within each site in each substrate, and confocal light scanning microscopy to assess the three-dimensional structure of the sampled biofilms. To gather further insights, we built a meta-community network and used its local realizations to analyze co-occurrence patterns of species. We found that light is a limiting factor in the baths environment, that moving along sites equals moving along an irradiation gradient, and that such gradient shapes the community structure, de facto separating a dark community, rich in Bacteria, Fungi and cyanobacteria, from two dim communities, rich in Chlorophyta. Almost all sites are dominated by photoautotrophs, with Fungi and Bacteria relegated to the role of rare species., and structural properties of biofilms are not consistent within the same substrate. We conclude that the Herculaneum suburban baths are an environment-shaped community, where one dark community (plaster) and one dim community (mortar) provides species to a "midway" community (marble).
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Project description:Streptococcus pneumoniaeis one of the key pathogens responsible for otitis media (OM), the most common infection in children and the largest cause of childhood antibiotic prescription. Novel therapeutic strategies that reduce the overall antibiotic consumption due to OM are required because, although widespread pneumococcal conjugate immunization has controlled invasive pneumococcal disease, overall OM incidence has not decreased. Biofilm formation represents an important phenotype contributing to the antibiotic tolerance and persistence ofS. pneumoniaein chronic or recurrent OM. We investigated the treatment of pneumococcal biofilms with nitric oxide (NO), an endogenous signaling molecule and therapeutic agent that has been demonstrated to trigger biofilm dispersal in other bacterial species. We hypothesized that addition of low concentrations of NO to pneumococcal biofilms would improve antibiotic efficacy and that higher concentrations exert direct antibacterial effects. Unlike in many other bacterial species, low concentrations of NO did not result inS. pneumoniaebiofilm dispersal. Instead, treatment of bothin vitrobiofilms andex vivoadenoid tissue samples (a reservoir forS. pneumoniaebiofilms) with low concentrations of NO enhanced pneumococcal killing when combined with amoxicillin-clavulanic acid, an antibiotic commonly used to treat chronic OM. Quantitative proteomic analysis using iTRAQ (isobaric tag for relative and absolute quantitation) identified 13 proteins that were differentially expressed following low-concentration NO treatment, 85% of which function in metabolism or translation. Treatment with low-concentration NO, therefore, appears to modulate pneumococcal metabolism and may represent a novel therapeutic approach to reduce antibiotic tolerance in pneumococcal biofilms.
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Project description:In nature, secondary metabolites mediate interactions between microorganisms residing in complex microbial communities. However, the degree to which community dynamics can be linked to secondary metabolite potential remains largely unknown. In this study, we address the relationship between community succession and secondary metabolism variation. We used 16S and 18S rRNA gene and adenylation domain amplicon sequencing, genome-resolved metagenomics, and untargeted metabolomics to track the taxons, biosynthetic gene clusters, and metabolome dynamics in situ of microorganisms during marine biofilm succession over 113 days. Two phases were identified during the community succession, with a clear shift around Day 29, where the alkaloid secondary metabolites, pseudanes, were also detected. The microbial secondary metabolite potential changed between the phases, and only a few community members, including Myxococotta spp., were responsible for the majority of the biosynthetic gene cluster potential in the early succession phase. In the late phase, bryozoans and benthic copepods were detected, and the microbial nonribosomal peptide potential drastically decreased in association with a reduction in the relative abundance of the prolific secondary metabolite producers. Conclusively, this study provides evidence that the early succession of the marine biofilm community favors prokaryotes with high nonribosomal peptide synthetase potential. In contrast, the late succession is dominated by multicellular eukaryotes and a reduction in bacterial nonribosomal peptide synthetase potential.
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Project description:The amino acid L-arginine inhibits bacterial coaggregation, is involved in cell-cell signaling, and alters bacterial metabolism in a broad range of species present in the human oral cavity. Given the range of effects of L-arginine on bacteria, we hypothesized that L-arginine might alter multi-species oral biofilm development and cause developed multi-species biofilms to disassemble. Because of these potential biofilm-destabilizing effects, we also hypothesized that L-arginine might enhance the efficacy of antimicrobials that normally cannot rapidly penetrate biofilms. A static microplate biofilm system and a controlled-flow microfluidic system were used to develop multi-species oral biofilms derived from pooled unfiltered cell-containing saliva (CCS) in pooled filter-sterilized cell-free saliva (CFS) at 37° C. The addition of pH neutral L-arginine monohydrochloride (LAHCl) to CFS was found to exert negligible antimicrobial effects but significantly altered biofilm architecture in a concentration-dependent manner. Under controlled flow, the biovolume of biofilms (?m(3)/?m(2)) developed in saliva containing 100-500 mM LAHCl were up to two orders of magnitude less than when developed without LAHCI. Culture-independent community analysis demonstrated that 500 mM LAHCl substantially altered biofilm species composition: the proportion of Streptococcus and Veillonella species increased and the proportion of Gram-negative bacteria such as Neisseria and Aggregatibacter species was reduced. Adding LAHCl to pre-formed biofilms also reduced biovolume, presumably by altering cell-cell interactions and causing cell detachment. Furthermore, supplementing 0.01% cetylpyridinium chloride (CPC), an antimicrobial commonly used for the treatment of dental plaque, with 500 mM LAHCl resulted in greater penetration of CPC into the biofilms and significantly greater killing compared to a non-supplemented 0.01% CPC solution. Collectively, this work demonstrates that LAHCl moderates multi-species oral biofilm development and community composition and enhances the activity of CPC. The incorporation of LAHCl into oral healthcare products may be useful for enhanced biofilm control.
| S-EPMC4422691 | biostudies-literature
Project description:Oral bacteria can influence the ability of Candida albicans to cause oropharyngeal candidiasis (OPC). We recently reported that a Lactobacillus johnsonii-enriched oral microbiota reduced C. albicans virulence in an immunosuppressed OPC mouse model. As a follow-up, in this work, we aimed to enrich the resident oral Lactobacillus communities with a prebiotic diet to further assess their effect on the severity of OPC. We tested the effect of a prebiotic xylo-oligosaccharides (XOS)-enriched diet in the oral global bacterial composition and severity of OPC. We assessed changes in the oral microbiome composition via 16S-rRNA gene high-throughput sequencing, validated by qPCR. The impact of the prebiotic diet on Candida infection was assessed by quantifying changes in oral fungal and bacterial biomass and scoring tongue lesions. Contrary to expectations, oral Lactobacillus communities were not enriched by the XOS-supplemented diet. Yet, XOS modulated the oral microbiome composition, increasing Bifidobacterium abundance and reducing enterococci and staphylococci. In the OPC model, the XOS diet attenuated Candida virulence and bacterial dysbiosis, increasing lactobacilli and reducing enterococci on the oral mucosa. We conclude that XOS attenuates Candida virulence by promoting a bacterial microbiome structure more resilient to Candida infection. IMPORTANCE This is the first study on the effects of a prebiotic diet on the oral mucosal bacterial microbiome and an oropharyngeal candidiasis (OPC) mouse model. We found that xylo-oligosaccharides change the oral bacterial community composition and attenuate OPC. Our results contribute to the understanding of the impact of the oral bacterial communities on Candida virulence.
| S-EPMC10580959 | biostudies-literature
Project description:Development of effective therapies to control oral biofilms is challenging, as topically introduced agents must avoid rapid clearance from biofilm-tooth interfaces while targeting biofilm microenvironments. Additionally, exopolysaccharides-matrix and acidification of biofilm microenvironments are associated with cariogenic (caries-producing) biofilm virulence. Thus, nanoparticle carriers capable of binding to hydroxyapatite (HA), saliva-coated HA (sHA), and exopolysaccharides with enhanced drug release at acidic pH were developed. Nanoparticles are formed from diblock copolymers composed of 2-(dimethylamino)ethyl methacrylate (DMAEMA), butyl methacrylate (BMA), and 2-propylacrylic acid (PAA) (p(DMAEMA)-b-p(DMAEMA-co-BMA-co-PAA)) that self-assemble into ∼21 nm cationic nanoparticles. Nanoparticles exhibit outstanding adsorption affinities (∼244 L-mmol(-1)) to negatively charged HA, sHA, and exopolysaccharide-coated sHA due to strong electrostatic interactions via multivalent tertiary amines of p(DMAEMA). Owing to hydrophobic cores, nanoparticles load farnesol, a hydrophobic antibacterial drug, at ∼22 wt %. Farnesol release is pH-dependent with t1/2 = 7 and 15 h for release at pH 4.5 and 7.2, as nanoparticles undergo core destabilization at acidic pH, characteristic of cariogenic biofilm microenvironments. Importantly, topical applications of farnesol-loaded nanoparticles disrupted Streptococcus mutans biofilms 4-fold more effectively than free farnesol. Mechanical stability of biofilms treated with drug-loaded nanoparticles was compromised, resulting in >2-fold enhancement in biofilm removal under shear stress compared to free farnesol and controls. Farnesol-loaded nanoparticles effectively attenuated biofilm virulence in vivo using a clinically relevant topical treatment regimen (2×/day) in a rodent dental caries disease model. Strikingly, treatment with farnesol-loaded nanoparticles reduced both the number and severity of carious lesions, while free farnesol had no effect. Nanoparticle carriers have great potential to enhance the efficacy of antibiofilm agents through multitargeted binding and pH-responsive drug release due to microenvironmental triggers.
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