Synergism between Corynebacterium and Streptococcus sanguinis reveals new interactions between oral commensals.
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ABSTRACT:
SUBMITTER: Treerat P
PROVIDER: S-EPMC7174362 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Polymicrobial biofilms are present in many environments particularly in the human oral cavity where they can prevent or facilitate the onset of disease. While recent advances have provided a clear picture of both the constituents and their biogeographic arrangement, it is still unclear what mechanisms of interaction occur between individual species in close proximity within these communities. In this study, we investigated two mechanisms of interaction between the highly abundant supragingival plaque (SUPP) commensal Corynebacterium matruchotii and Streptococcus mitis which are directly adjacent/attached in vivo. We discovered that C. matruchotii enhanced the fitness of streptococci dependent on its ability to detoxify streptococcal-produced hydrogen peroxide and its ability to oxidize lactate also produced by streptococci. We demonstrate that the fitness of adjacent streptococci was linked to that of C. matruchotii and that these mechanisms support the previously described "corncob" arrangement between these species but that this is favorable only in aerobic conditions. Furthermore, we utilized scanning electrochemical microscopy to quantify lactate production and consumption between individual bacterial cells for the first time, revealing that lactate oxidation provides a fitness benefit to S. mitis not due to pH mitigation. This study describes mechanistic interactions between two highly abundant human commensals that can explain their observed in vivo spatial arrangements and suggest a way by which they may help preserve a healthy oral bacterial community. IMPORTANCE As the microbiome era matures, the need for mechanistic interaction data between species is crucial to understand how stable microbiomes are preserved, especially in healthy conditions where the microbiota could help resist opportunistic or exogenous pathogens. Here we reveal multiple mechanisms of interaction between two commensals that dictate their biogeographic relationship to each other in previously described structures in human supragingival plaque. Using a novel variation for chemical detection, we observed metabolite exchange between individual bacterial cells in real time validating the ability of these organisms to carry out metabolic crossfeeding at distal and temporal scales observed in vivo. These findings reveal one way by which these interactions are both favorable to the interacting commensals and potentially the host.
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Project description:Airway infections associated with cystic fibrosis (CF) are polymicrobial. We reported previously that clinical isolates of Pseudomonas aeruginosa promote the growth of a variety of streptococcal species. To explore the mechanistic basis of this interaction, we performed a genetic screen to identify mutants of Streptococcus sanginuis SK36 whose growth was no longer enhanced by P. aeruginosa PAO1. Mutations in the zinc uptake systems of S. sanguinis SK36 reduced growth of these strains by 1 to 3 logs compared to that of wild-type S. sanguinis SK36 when grown in coculture with P. aeruginosa PAO1, and exogenous zinc (0.1 to 10 μM) rescued the coculture defect of zinc uptake mutants of S. sanguinis SK36. Zinc uptake mutants of S. sanguinis SK36 had no obvious growth defect in monoculture. Consistent with competition for zinc driving coculture dynamics, S. sanguinis SK36 grown in coculture with P. aeruginosa showed increased expression of zinc uptake genes compared to that of S. sanguinis grown alone. Strains of P. aeruginosa PAO1 defective in zinc transport also supported ∼2-fold more growth by S. sanguinis compared to that in coculture with wild-type P. aeruginosa PAO1. An analysis of 118 CF sputum samples revealed that total zinc levels varied from ∼5 to 145 μM. At relatively low zinc levels, Pseudomonas and Streptococcus spp. were found in approximately equal abundance; at higher zinc levels, we observed a decline in relative abundance of Streptococcus spp., perhaps as a result of increasing zinc toxicity. Together, our data indicate that the relative abundances of these microbes in the CF airway may be impacted by zinc levels.IMPORTANCE Polymicrobial infections in CF cases likely impact patient health, but the mechanism(s) underlying such interactions is poorly understood. Here, we show using an in vitro model system that interactions between Pseudomonas and Streptococcus are modulated by zinc availability, and clinical data are consistent with this model. Together with previous studies, our work supports a role for metal homeostasis as a key factor driving microbial interactions.
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Project description:In this study, the effect of bacterial multispecies communities on the adhesion of Streptococcus mutans and Streptococcus sanguinis to dental restorative material was investigated. The saliva-coated specimens of zirconia and composite were incubated with the following combinations: single species, S. mutans or S. sanguinis; two species, single species combined with other oral streptococci; multiple species, combination of Actinomyces naeslundii, Fusobacterium nucleatum, and Prevotella ssp.; and the two-species combinations. The adherent bacteria were counted after plating of serial dilutions. Effects of material and bacteria on adhesion of S. mutans and S. sanguinis were evaluated with multiple linear regression analyses. No significant differences between the materials regarding the adhesion of S. mutans and S. sanguinis were observed. The adhesion of S. mutans was negatively influenced by the presence of other streptococci. Enhancing effects (610.6%) were seen in the presence of Prevotella intermedia. The adhesion of S. sanguinis decreased in the presence of other bacteria, except F. nucleatum (increase of 717.4%). Significant inhibitory effects were detected in the presence of S. mutans and A. naeslundii (reduction of 95.9% and 78.5%, respectively). The results of this study suggest that adhesion of both types of streptococci to restorative materials is influenced by various bacterial interactions.
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Project description:Polymicrobial interactions with oral mucosal surfaces determine the health status of the host. While a homeostatic balance provides protection from oral disease, a dysbiotic polymicrobial community promotes tissue destruction and chronic oral diseases. How polymicrobial communities transition from a homeostatic to a dysbiotic state is an understudied process. Thus, we were interested to investigate this ecological transition by focusing on biofilm communities containing high abundance commensal species and low abundance pathobionts to characterize the host-microbiome interactions occurring during oral health. To this end, a multispecies biofilm model was examined using the commensal species Corynebacterium durum and Streptococcus sanguinis and the pathobiont Porphyromonas gingivalis. We compared how both single and multispecies biofilms interact with different oral mucosal and gingival cell types, including the well-studied oral keratinocyte cell lines OKF4/TERT-1and hTERT TIGKs as well as human primary periodontal ligament cells. While single species biofilms of C. durum, S. sanguinis, and P. gingivalis are all characterized by unique cytokine responses for each species, multispecies biofilms elicited a response resembling S. sanguinis single species biofilms. One notable exception is the influence of P. gingivalis upon TNF-α and Gro-α production in hTERT TIGKs cells, which was not affected by the presence of other species. This study is also the first to examine the host response to C. durum. Interestingly, C. durum yielded no notable inflammatory responses from any of the tested host cells, suggesting it functions as a true commensal species. Conversely, S. sanguinis was able to induce expression and secretion of the proinflammatory cytokines IL-6 and IL-8, demonstrating a much greater inflammatory potential, despite being health associated. Our study also demonstrates the variability of host cell responses between different cell lines, highlighting the importance of developing relevant in vitro models to study oral microbiome-host interactions.
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Project description:The novel 3-methyladenine DNA glycosylase enzyme from oral pathogen Streptococcus sanguinisin involves in DNA repair mechanisms and participates in base excision repair. Its 3D structure is still unknown which may be a potential drug target, therefore here we proposed its putative 3D structure by homology modeling approach. EsyPred3d software produced more precise modeled structure as compare to Swiss model software. The modeled structure was further verified by PROCHECK analysis and subjected to functional site prediction servers for active site residues prediction. The functional site was further validated by molecular docking approach with ligand EDA (3- [2- Deoxyribofuranosyl] - 3H- 1, 3, 4, 5A, 8-Pentaaza- Asindacene-5- monophosphate) from 1F4R. The EDR docked at the cavity of modeled structure of 3-methyladenine DNA glycosylase enzyme with highest Patchdock score of 3966 and lowest Autodock 4 docking energy of -10.30 Kcal/mol. The YA51, LA105, RA107 residues are surrounding the EDA and matching with ligand binding residues predicted by PROFUNC server.
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Project description:Streptococcus gordonii and Streptococcus sanguinis belong to the Mitis group streptococci, which mostly are commensals in the human oral cavity. Though they are oral commensals, they can escape their niche and cause infective endocarditis, a severe infection with high mortality. Several virulence factors important for the development of infective endocarditis have been described in these two species. However, the background for how the commensal bacteria, in some cases, become pathogenic is still not known. To gain a greater understanding of the mechanisms of the pathogenic potential, we performed a comparative analysis of 38 blood culture strains, S. sanguinis (n = 20) and S. gordonii (n = 18) from patients with verified infective endocarditis, along with 21 publicly available oral isolates from healthy individuals, S. sanguinis (n = 12) and S. gordonii (n = 9). Using whole genome sequencing data of the 59 streptococci genomes, functional profiles were constructed, using protein domain predictions based on the translated genes. These functional profiles were used for clustering, phylogenetics and machine learning. A clear separation could be made between the two species. No clear differences between oral isolates and clinical infective endocarditis isolates were found in any of the 675 translated core-genes. Additionally, random forest-based machine learning and clustering of the pan-genome data as well as amino acid variations in the core-genome could not separate the clinical and oral isolates. A total of 151 different virulence genes was identified in the 59 genomes. Among these homologs of genes important for adhesion and evasion of the immune system were found in all of the strains. Based on the functional profiles and virulence gene content of the genomes, we believe that all analysed strains had the ability to become pathogenic.
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Project description:Streptococcus sanguinis, an abundant and benign inhabitant of the oral cavity, is an important etiologic agent of infective endocarditis (IE), particularly in people with predisposing cardiac valvular damage. Although commonly isolated from patients with IE, little is known about the factors that make any particular S. sanguinis isolate more virulent than another or, indeed, whether significant differences in virulence exist among isolates. In this study, we compared the genomes of a collection of S. sanguinis strains comprised of both oral isolates and bloodstream isolates from patients diagnosed with IE. Oral and IE isolates could not be distinguished by phylogenetic analyses, and we did not succeed in identifying virulence genes unique to the IE strains. We then investigated the virulence of these strains in a rabbit model of IE using a variation of the Bar-seq (barcode sequencing) method wherein we pooled the strains and used Illumina sequencing to count unique barcodes that had been inserted into each isolate at a conserved intergenic region. After we determined that several of the genome sequences were misidentified in GenBank, our virulence results were used to inform our bioinformatic analyses, identifying genes that may explain the heterogeneity in virulence. We further characterized these strains by assaying for phenotypes potentially contributing to virulence. Neither strain competition via bacteriocin production nor biofilm formation showed any apparent relationship with virulence. Increased cell-associated manganese was, however, correlated with blood isolates. These results, combined with additional phenotypic assays, suggest that S. sanguinis virulence is highly variable and results from multiple genetic factors.
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Project description:N-Acetylglucosamine (GlcNAc) and glucosamine (GlcN) enhance the competitiveness of the laboratory strain DL1 of Streptococcus gordonii against the caries pathogen Streptococcus mutans Here, we examine how amino sugars affect the interaction of five low-passage-number clinical isolates of abundant commensal streptococci with S. mutans by utilizing a dual-species biofilm model. Compared to that for glucose, growth on GlcN or GlcNAc significantly reduced the viability of S. mutans in cocultures with most commensals, shifting the proportions of species. Consistent with these results, production of H2O2 was increased in most commensals when growing on amino sugars, and inhibition of S. mutans by Streptococcus cristatus, Streptococcus oralis, or S. gordonii was enhanced by amino sugars on agar plates. All commensals except S. oralis had higher arginine deiminase activities when grown on GlcN and, in some cases, GlcNAc. In ex vivo biofilms formed using pooled cell-containing saliva (CCS), the proportions of S. mutans were drastically diminished when GlcNAc was the primary carbohydrate. Increased production of H2O2 could account in large part for the inhibitory effects of CCS biofilms. Surprisingly, amino sugars appeared to improve mutacin production by S. mutans on agar plates, suggesting that the commensals have mechanisms to actively subvert antagonism by S. mutans in cocultures. Collectively, these findings demonstrate that amino sugars can enhance the beneficial properties of low-passage-number commensal oral streptococci and highlight their potential for moderating the cariogenicity of oral biofilms.IMPORTANCE Dental caries is driven by dysbiosis of oral biofilms in which dominance by acid-producing and acid-tolerant bacteria results in loss of tooth mineral. Our previous work demonstrated the beneficial effects of amino sugars GlcNAc and GlcN in promoting the antagonistic properties of a health-associated oral bacterium, Streptococcus gordonii, in competition with the major caries pathogen Streptococcus mutans Here, we investigated 5 low-passage-number clinical isolates of the most common streptococcal species to establish how amino sugars may influence the ecology and virulence of oral biofilms. Using multiple in vitro models, including a human saliva-derived microcosm biofilm, experiments showed significant enhancement by at least one amino sugar in the ability of most of these bacteria to suppress the caries pathogen. Therefore, our findings demonstrated the mechanism of action by which amino sugars may affect human oral biofilms to promote health.
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