Multi-omics Analyses Reveal Synergistic Carbohydrate Metabolism in Streptococcus mutans-Candida albicans Mixed-Species Biofilms

Ellepola, Kassapa; Truong, Tin; Liu, Yuan; Lin, Qifeng; Lim, Teck Kwang; Lee, Yew Mun; Cao, Tong; Koo, Hyun; Seneviratne, Chaminda Jayampath

doi:10.1128/iai.00339-19

Cited by 75 publications

(86 citation statements)

References 49 publications

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“…Mnn9, Van1, and Pmr1 contribute to mannan production, while Gca1 and Big1 regulate β-glucan synthesis (Mitchell et al, 2015), and the expression of genes was correlated with the synthesis of exopolysaccharide. Previous studies reported that S. mutans-derived GtfB binds to C. albicans surface mannan (Hwang et al, 2015), transcriptomic analysis of S. mutans-C. albicans mixed biofilms reveals that S. mutans enhances C. albicans carbohydrate metabolism and alters mannan and glucan production of C. albicans (Ellepola et al, 2019), and the C. albicans biofilm polysaccharide production results showed that exopolysaccharide levels and C. albicans secreted β-glucans were significantly increased in the S. mutans MV-treated group. These results are consistent with the observed upregulation in the expression of the abovementioned C. albicans genes.…”

Section: Discussionmentioning

confidence: 78%

Streptococcus mutans Membrane Vesicles Harboring Glucosyltransferases Augment Candida albicans Biofilm Development

Tao

Cao

et al. 2020

Front. Microbiol.

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Candida albicans, as the most common fungus in the oral cavity, is often detected in early childhood caries. Streptococcus mutans is the major etiological agent of dental caries, but the role of S. mutans on C. albicans growth and biofilm development remains to be elucidated. Membrane vesicles (MVs) are a cell-secreted subcellular fraction that play an important role in intercellular communication and disease progression. In the present study, we investigated whether MVs from S. mutans augment C. albicans growth and biofilm development. The results indicated that S. mutans MVs augmented C. albicans biofilm development but had no significant effect on C. albicans growth under planktonic conditions. Subsequently, we labeled S. mutans MVs with PKH26 and used confocal laser scanning microscopy (CLSM) to track S. mutans MVs, which were observed to be located in the C. albicans biofilm extracellular matrix. Monosaccharide tests showed that S. mutans MVs contribute to sucrose metabolism in C. albicans. Polysaccharides were significantly enriched in the S. mutans MV-treated group. MVs from gtfBC mutant strains were compared with those from the wild-type S. mutans. The results revealed that MVs from the gtfBC mutant had no effect on C. albicans biofilm formation and exopolysaccharide production. In addition, C. albicans biofilm transcriptional regulators (Ndt80, Als1, Mnn9, Van1, Pmr1, Gca1, and Big1) expression were upregulated in S. mutans MV-treated group. In summary, the results of the present study showed that S. mutans MVs harboring glucosyltransferases involved in exopolysaccharide production augment C. albicans biofilm development, revealing a key role for S. mutans MVs in cross-kingdom interactions between S. mutans and C. albicans.

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Section: Discussionmentioning

confidence: 78%

Streptococcus mutans Membrane Vesicles Harboring Glucosyltransferases Augment Candida albicans Biofilm Development

Tao

Cao

et al. 2020

Front. Microbiol.

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“…Studies have shown that C. albicans is aciduric and acidogenic and is capable of biofilm formation, especially when grown in culture with S. mutans, resulting in increased amounts of extracellular polysaccharides (EPS) pertinent for caries development (23,29,40,81). Recent meta-omic analyses of S. mutans and C. albicans grown in mixed biofilms have provided molecular evidence to support the hypothesis that C. albicans enhances the cariogenic potential of S. mutans (28).…”

Section: Discussionmentioning

confidence: 99%

Site-Specific Profiling of the Dental Mycobiome Reveals Strong Taxonomic Shifts during Progression of Early-Childhood Caries

O’Connell

Santos

Springer

et al. 2020

Appl Environ Microbiol

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Dental caries is one of the most common diseases worldwide. Bacteria and fungi are both commensals in the oral cavity; however, most research regarding caries has focused on bacterial impacts. The oral fungal mycobiome associated with caries is not well characterized, and its role in disease is unclear. ITS1 amplicon sequencing was used to generate taxonomic profiles from site-specific supragingival plaque samples (n = 82) obtained from 33 children with different caries status. Children were either caries free (CF), caries active with enamel lesions (CAE), or caries active with dentin lesions (CA). Plaque samples were collected from caries-free surfaces (PF) and from enamel (PE) and dentin (PD) lesions. Taxonomic profiles representing the different categorizations (CF-PF, CAE-PF, CAE-PE, CA-PF, CA-PE, and CA-PD) were used to characterize the mycobiome and its change through disease progression. A total of 139 fungal species were identified. Candida albicans was the most abundant species, followed by Candida dubliniensis. We found that severely progressed plaque communities (CA-PD) were significantly different from healthy plaque communities (CF-PF). A total of 32 taxa were differentially abundant across the plaque categories. C. albicans, C. dubliniensis, Nigrospora oryzae, and an unclassified Microdochium sp. were correlated with caries, whereas 12 other taxa were correlated with health. C. dubliniensis increased steadily as caries progressed, suggesting that C. dubliniensis may play an important role in caries pathogenicity. In contrast, four health-associated fungal taxa have the potential to antagonize the cariogen Streptococcus mutans via xylitol production, suggesting a possible fungal mechanism that could contribute to maintenance of dental health. IMPORTANCE Early-childhood caries is one of the most prevalent diseases in children worldwide and, while preventable, remains a global public health concern. Untreated cavities are painful and expensive and can lead to tooth loss and a lower quality of life. Caries are driven by acid production via microbial fermentation of dietary carbohydrates, resulting in enamel erosion. While caries is a well-studied disease, most research has focused on bacterial impacts, even though fungi are commensal organisms living within the plaque biofilm. There is very little known about how fungi impact caries pathogenicity. The elucidation of fungal taxa involved in caries disease progression is necessary for a more holistic view of the human oral microbiome. Data from this study will improve our understanding of how the fungal community changes as disease progresses and provide insight into the complex etiology of dental caries, which is necessary for the development of treatment plans and preventative measures.

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“…These glucans in turn increase the binding sites for S. mutans [13,17] resulting in a highly pathogenic mixed-species biofilm [15]. We demonstrated that S. mutans derived GtfB is able to augment the accumulation of C. albicans in mixed-species biofilms and enhance C. albicans growth by cross-feeding of glucose and fructose by sucrose breakdown [18,19]. Moreover, S. mutans was able to up-regulate the expression of C. albicans hypha associated genes such as HWP1, ALS1 and ALS3 which can be attributed to an increase in virulence of the organism in mixed-species biofilms.…”

Section: Introductionmentioning

confidence: 88%

Lactobacillus Plantarum 108 Inhibits Streptococcus mutans and Candida albicans Mixed-Species Biofilm Formation

et al. 2020

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Streptococcus mutans is the principal biofilm forming oral pathogen associated with dental caries. Studies have shown that Candida albicans, a commensal oral fungus is capable of forming pathogenic mixed-species biofilms with S. mutans. The treatment of bacterial and fungal infections using conventional antimicrobial agents has become challenging due to the antimicrobial resistance of the biofilm mode of growth. The present study aimed to evaluate the efficacy of secretory components of Lactobacillus plantarum 108, a potentially promising probiotic strain, against S. mutans and C. albicans single and mixed-species biofilms. L. plantarum 108 supernatant inhibited S. mutans and C. albicans single-species biofilms as shown by XTT reduction assay, crystal violet assay, and colony forming units counting. The probiotic supernatant significantly inhibited the S. mutans and C. albicans mixed-species biofilm formation. The pre-formed mixed-species biofilms were also successfully reduced. Confocal microscopy showed poorly developed biofilm architecture in the probiotic supernatant treated biofilms. Moreover, the expression of S. mutans genes associated with glucosyltransferase activity and C. albicans hyphal specific genes (HWP1, ALS1 and ALS3) were down-regulated in the presence of the probiotic supernatant. Altogether, the data demonstrated the capacity of L. plantarum 108 supernatant to inhibit the S. mutans and C. albicans mixed-species biofilms. Herein, we provide a new insight on the potential of probiotic-based strategies to prevent bacterial-fungal mixed-species biofilms associated with dental caries.

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Multi-omics Analyses Reveal Synergistic Carbohydrate Metabolism in Streptococcus mutans-Candida albicans Mixed-Species Biofilms

Cited by 75 publications

References 49 publications

Streptococcus mutans Membrane Vesicles Harboring Glucosyltransferases Augment Candida albicans Biofilm Development

Streptococcus mutans Membrane Vesicles Harboring Glucosyltransferases Augment Candida albicans Biofilm Development

Site-Specific Profiling of the Dental Mycobiome Reveals Strong Taxonomic Shifts during Progression of Early-Childhood Caries

Lactobacillus Plantarum 108 Inhibits Streptococcus mutans and Candida albicans Mixed-Species Biofilm Formation

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