Dataset Information

Streptococcus mutans adhesion force sensing in multi-species oral biofilms.

ABSTRACT: Bacteria utilize chemical and mechanical mechanisms to sense their environment, to survive hostile conditions. In mechanical sensing, intra-bilayer pressure profiles change due to deformation induced by the adhesion forces bacteria experience on a surface. Emergent properties in mono-species Streptococcus mutans biofilms, such as extracellular matrix production, depend on the adhesion forces that streptococci sense. Here we determined whether and how salivary-conditioning film (SCF) adsorption and the multi-species nature of oral biofilm influence adhesion force sensing and associated gene expression by S. mutans. Hereto, Streptococcus oralis, Actinomyces naeslundii, and S. mutans were grown together on different surfaces in the absence and presence of an adsorbed SCF. Atomic force microscopy and RT-qPCR were used to measure S. mutans adhesion forces and gene expressions. Upon SCF adsorption, stationary adhesion forces decreased on a hydrophobic and increased on a hydrophilic surface to around 8?nN. Optical coherence tomography showed that triple-species biofilms on SCF-coated surfaces with dead S. oralis adhered weakly and often detached as a contiguous sheet. Concurrently, S. mutans displayed no differential adhesion force sensing on SCF-coated surfaces in the triple-species biofilms with dead S. oralis, but once live S. oralis were present S. mutans adhesion force sensing and gene expression ranked similar as on surfaces in the absence of an adsorbed SCF. Concluding, live S. oralis may enzymatically degrade SCF components to facilitate direct contact of biofilm inhabitants with surfaces and allow S. mutans adhesion force sensing of underlying surfaces to define its appropriate adaptive response. This represents a new function of initial colonizers in multi-species oral biofilms.

SUBMITTER: Wang C

PROVIDER: S-EPMC7314845 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Streptococcus mutans adhesion force sensing in multi-species oral biofilms.

Wang Can C van der Mei Henny C HC Busscher Henk J HJ Ren Yijin Y

NPJ biofilms and microbiomes 20200624 1

Bacteria utilize chemical and mechanical mechanisms to sense their environment, to survive hostile conditions. In mechanical sensing, intra-bilayer pressure profiles change due to deformation induced by the adhesion forces bacteria experience on a surface. Emergent properties in mono-species Streptococcus mutans biofilms, such as extracellular matrix production, depend on the adhesion forces that streptococci sense. Here we determined whether and how salivary-conditioning film (SCF) adsorption a ...[more]

PMID: 32581220

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Project description:Unlabelledl-Arginine, a ubiquitous amino acid in human saliva, serves as a substrate for alkali production by arginolytic bacteria. Recently, exogenous l-arginine has been shown to enhance the alkalinogenic potential of oral biofilm and destabilize its microbial community, which might help control dental caries. However, l-arginine exposure may inflict additional changes in the biofilm milieu when bacteria are growing under cariogenic conditions. Here, we investigated how exogenous l-arginine modulates biofilm development using a mixed-species model containing both cariogenic (Streptococcus mutans) and arginolytic (Streptococcus gordonii) bacteria in the presence of sucrose. We observed that 1.5% (wt/vol) l-arginine (also a clinically effective concentration) exposure suppressed the outgrowth of S. mutans, favored S. gordonii dominance, and maintained Actinomyces naeslundii growth within biofilms (versus vehicle control). In parallel, topical l-arginine treatments substantially reduced the amounts of insoluble exopolysaccharides (EPS) by >3-fold, which significantly altered the three-dimensional (3D) architecture of the biofilm. Intriguingly, l-arginine repressed S. mutans genes associated with insoluble EPS (gtfB) and bacteriocin (SMU.150) production, while spxB expression (H2O2 production) by S. gordonii increased sharply during biofilm development, which resulted in higher H2O2 levels in arginine-treated biofilms. These modifications resulted in a markedly defective EPS matrix and areas devoid of any bacterial clusters (microcolonies) on the apatitic surface, while the in situ pH values at the biofilm-apatite interface were nearly one unit higher in arginine-treated biofilms (versus the vehicle control). Our data reveal new biological properties of l-arginine that impact biofilm matrix assembly and the dynamic microbial interactions associated with pathogenic biofilm development, indicating the multiaction potency of this promising biofilm disruptor.ImportanceDental caries is one of the most prevalent and costly infectious diseases worldwide, caused by a biofilm formed on tooth surfaces. Novel strategies that compromise the ability of virulent species to assemble and maintain pathogenic biofilms could be an effective alternative to conventional antimicrobials that indiscriminately kill other oral species, including commensal bacteria. l-Arginine at 1.5% has been shown to be clinically effective in modulating cariogenic biofilms via alkali production by arginolytic bacteria. Using a mixed-species ecological model, we show new mechanisms by which l-arginine disrupts the process of biofilm matrix assembly and the dynamic microbial interactions that are associated with cariogenic biofilm development, without impacting the bacterial viability. These results may aid in the development of enhanced methods to control biofilms using l-arginine.

Project description:Biofilms consist of bacterial cells surrounded by a matrix of extracellular polymeric substance (EPS), which protects the colony from many countermeasures, including antibiotic treatments. Growth and formation of bacterial biofilms are affected by nutrients available in the environment. In the oral cavity, the presence of sucrose affects the growth of Streptococcus mutans that produce acids that erode enamel and form dental caries. Biofilm formation on dental implants commonly leads to severe infections and can restrict osseointegration necessary for the implant to be successful. This work determines the effect of sucrose concentration on biofilm EPS formation and adhesion of Streptococcus mutans, a common oral colonizer, to titanium substrates simulating common dental implants. Biofilm formation and profiles are visualized at high magnification with scanning electron microscopy (SEM). Large mounds and complex structures consisting of bacterial cells and EPS can be seen in biofilms at sucrose concentrations that are favorable for biofilm growth. The laser spallation technique is used to apply stress wave loading to the biofilm, causing the biofilm to delaminate at a critical tensile stress threshold. The critical tensile stress threshold is the adhesion strength. Because laser spallation applies the stress loading to the rear of the substrate, bulk adhesion properties of the biofilm can be determined despite the heterogenous composition and low cohesion strength of the biofilm. Statistical analysis reveals that adhesion strength of biofilms initially increase with increasing sucrose concentration and then decrease as sucrose concentration continues to increase. The adhesion strength of bacterial biofilms to the substrate in this study is compared to the adhesion of osteoblast-like cells to the same substrates published previously. When sucrose is present in the biofilm growth environment, S. mutans adhesion is higher than that of the osteoblast-like cells. Results of this study suggest sucrose-mediated S. mutans biofilms may outcompete osteoblasts in terms of adhesion during osseointegration, which could explain higher rates of peri-implant disease associated with high sugar diets. Further studies demonstrating adhesion differentials between biofilms and cells including co-cultures are needed and motivated by the present work.

Dataset Information

Streptococcus mutans adhesion force sensing in multi-species oral biofilms.

Publications

Streptococcus mutans adhesion force sensing in multi-species oral biofilms.

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