Understanding the Matrix: The Role of Extracellular DNA in Oral Biofilms

Serrage, Hannah; Jepson, Mark A.; Rostami, Nadia; Jakubovics, Nicholas S.; Nobbs, Angela H.

doi:10.3389/froh.2021.640129

Cited by 19 publications

(17 citation statements)

References 77 publications

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“…Our experiments provide evidence that, by increasing the amount of eDNA, some antibiotic treatments could enhance the formation of biofilms by promoting the occurrence of streamers which, given their spatial localization, eventually lead to clogging in medical devices such as stents or catheters and to the spreading of infection due to biofilm detachment. Moreover, since it is becoming clear that bacterial eDNA plays an important role in potentiating inflammation ( 77 , 78 ), these findings are paving the way for future studies on the effects of antibiotic treatments on biofilm-forming pathogens and the host immune response.…”

Section: Discussionmentioning

confidence: 99%

The structural role of bacterial eDNA in the formation of biofilm streamers

Secchi

Savorana

Vitale

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Significance Streamers, filamentous bacterial biofilms formed in flowing systems, are ubiquitous in natural and artificial environments, where they cause clogging of devices and spreading of infections. Despite their impact, little is known about the nature and properties of streamers and their response to fluid flow. Here, we uncover the specific contribution of bacterial secreted extracellular DNA and exopolysaccharide Pel, two important components in Pseudomonas aeruginosa biofilms, to the formation and the mechanical properties of the streamers. We then show how this knowledge can be used to control biofilm streamer formation, both to inhibit or to promote it.

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Section: Discussionmentioning

confidence: 99%

The structural role of bacterial eDNA in the formation of biofilm streamers

Secchi

Savorana

Vitale

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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“…There is evidence that eDNA can enhance the adhesion of S. mutans to hydrophobic surfaces and subsequently increase the viscoelasticity of the biofilms [ 6 – 8 , 58 ]. aPDT using Emo-CS-NPs led to a significant reduction of eDNA levels.…”

Section: Discussionmentioning

confidence: 99%

“…As biofilm formation progresses, microbial species can produce and encase themselves within the extracellular polymeric substance comprised a network of molecules such as polysaccharides, lipids, proteins, and extracellular DNA (eDNA) [ 6 ]. The studies focusing on S. mutans confirm the role of eDNA in maintaining biofilm structural integrity and stability [ 7 , 8 ], consistent with findings for other bacterial species [ 9 – 11 ].…”

Section: Introductionmentioning

confidence: 99%

Theranostic nanoplatforms of emodin-chitosan with blue laser light on enhancing the anti-biofilm activity of photodynamic therapy against Streptococcus mutans biofilms on the enamel surface

2022

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Background Combining photosensitizer and light irradiation, named antimicrobial photodynamic therapy (aPDT) is an adjuvant therapy for eliminating microbial biofilms. This ex vivo study evaluates the effect of anti-biofilm activity of aPDT based on emodin-chitosan nanoparticles (Emo-CS-NPs) plus blue laser light against Streptococcus mutans biofilm on the enamel surface. Materials After determination of the fractional inhibitory concentration index of Emo and CS by checkerboard array assay, Emo-CS-NPs were synthesized and characterized. Following treatment of pre-formed S. mutans biofilms on the enamel slabs, cellular uptake of Emo-CS-NPs and intracellular reactive oxygen species (ROS) production were determined. The anti-biofilm and anti-metabolic activities of aPDT were investigated. Eventually, lactic acid production capacity, concentrations of S. mutans extracellular DNA (eDNA) levels, and expression of the gene involved in the biofilm formation (gtfB) were evaluated. Results The maximum uptake of Emo-CS-NPs occurs in an incubation time of 5 min. When irradiated, Emo-CS-NPs were photoactivated, generating ROS, and led to a decrease in the cell viability and metabolic activity of S. mutans significantly (P < 0.05). S. mutans eDNA and lactic acid production outcomes indicated that Emo-CS-NPs-mediated aPDT led to a significant reduction of eDNA levels (48%) and lactic acid production (72.4%) compared to the control group (P < 0.05). In addition, gtfB mRNA expression in S. mutans was downregulated (7.8-fold) after aPDT in comparison with the control group (P < 0.05). Conclusions Our data support that, aPDT using Emo-CS-NPs revealed the highest cellular uptake and ROS generation. Emo-CS-NPs based aPDT could inhibit significantly biofilm formation and reduce effectively virulence potency of S. mutans; thus, it could be an adjuvant therapy against dental caries.

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“…Our experiments provide further and stronger evidence that, by increasing the amount of eDNA, some antibiotic treatments could enhance the formation of biofilms by promoting the occurrence of streamers which, given their spatial localization, eventually lead to clogging in medical devices such as stents or catheters and to the spreading of infection due to biofilm detachment. Moreover, since it is becoming clear that bacterial eDNA plays an important role in potentiating inflammation (71,72), these findings are paving the way for future studies on the effects of antibiotic treatments on biofilm-forming pathogens and the host immune response.…”

Section: Discussionmentioning

confidence: 99%

The structural role of bacterial eDNA in the formation of biofilm streamers

Secchi

Savorana

Vitale

et al. 2021

Preprint

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Across diverse habitats, bacteria are mainly found as biofilms, surface-attached communities embedded in a self-secreted matrix of extracellular polymeric substances (EPS), which enhances bacterial resistance to antimicrobial treatment and mechanical stresses. In the presence of flow and geometric constraints such as corners or constrictions, biofilms take the form of long, suspended threads known as streamers, which bear important consequences in industrial and clinical settings by causing clogging and fouling. The formation of streamers is thought to be driven by the viscoelastic nature of the biofilm matrix. Yet, little is known about the structural composition of streamers and how it affects their mechanical properties. Here, using a microfluidic platform that allows growing and precisely examining biofilm streamers, we show that extracellular DNA (eDNA) constitutes the backbone and is essential for the mechanical stability of Pseudomonas aeruginosa' s streamers. This finding is supported by the observations that DNA-degrading enzymes prevent the formation of streamers and clear already formed ones, and that the antibiotic ciprofloxacin promotes their formation by increasing the release of eDNA. Furthermore, using mutants for production of the exopolysaccharide Pel, an important component of P. aeruginosa' s EPS, we reveal a new, although indirect role of Pel, in tuning the mechanical properties of the streamers. Taken together, these results highlight the importance of eDNA and of its interplay with Pel in determining the mechanical properties of P. aeruginosa streamers, and suggest that targeting the composition of streamers can be an effective approach to control the formation of these biofilm structures.

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Understanding the Matrix: The Role of Extracellular DNA in Oral Biofilms

Cited by 19 publications

References 77 publications

The structural role of bacterial eDNA in the formation of biofilm streamers

The structural role of bacterial eDNA in the formation of biofilm streamers

Theranostic nanoplatforms of emodin-chitosan with blue laser light on enhancing the anti-biofilm activity of photodynamic therapy against Streptococcus mutans biofilms on the enamel surface

The structural role of bacterial eDNA in the formation of biofilm streamers

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