The exopolysaccharide\u2013eDNA interaction modulates 3D architecture of Bacillus subtilis biofilm

Na Peng,Monika Mortimer,Qiaoyun Huang,Chunhui Gao,Peng Cai,Yichao Wu

doi:10.1186/s12866-020-01789-5

Na Peng, Monika Mortimer + Show 4 more

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https://doi.org/10.1186/s12866-020-01789-5

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Abstract

BackgroundBacterial biofilms are surface-adherent microbial communities in which individual cells are surrounded by a self-produced extracellular matrix of polysaccharides, extracellular DNA (eDNA) and proteins. Interactions among matrix components within biofilms are responsible for creating an adaptable structure during biofilm development. However, it is unclear how the interactions among matrix components contribute to the construction of the three-dimensional (3D) biofilm architecture.ResultsDNase I treatment significantly inhibited Bacillus subtilis biofilm formation in the early phases of biofilm development. Confocal laser scanning microscopy (CLSM) and image analysis revealed that eDNA was cooperative with exopolysaccharide (EPS) in the early stages of B. subtilis biofilm development, while EPS played a major structural role in the later stages. In addition, deletion of the EPS production gene epsG in B. subtilis SBE1 resulted in loss of the interaction between EPS and eDNA and reduced the biofilm biomass in pellicles at the air-liquid interface. The physical interaction between these two essential biofilm matrix components was confirmed by isothermal titration calorimetry (ITC).ConclusionsBiofilm 3D structures become interconnected through surrounding eDNA and EPS. eDNA interacts with EPS in the early phases of biofilm development, while EPS mainly participates in the maturation of biofilms. The findings of this study provide a better understanding of the role of the interaction between eDNA and EPS in shaping the biofilm 3D matrix structure and biofilm formation.

Highlights

Bacterial biofilms are surface-adherent microbial communities in which individual cells are surrounded by a self-produced extracellular matrix of polysaccharides, extracellular DNA and proteins
The role of extracellular DNA in the construction of the B. subtilis SBE1 biofilm three-dimensional (3D) architecture In order to understand the contribution of eDNA in the biofilm formation of B. subtilis SBE1, the impact of DNase I on biofilm formation was tested using a static deeper than those formed in the absence of DNase I (Fig. 2c, d and e) (P < 0.001), suggesting that the gaps between cells in biofilms may be filled with eDNA
Imaris analysis showed that the content of eDNA in the biofilms was substantially reduced after 24 h (Fig. 4b)

Summary

Introduction

Bacterial biofilms are surface-adherent microbial communities in which individual cells are surrounded by a self-produced extracellular matrix of polysaccharides, extracellular DNA (eDNA) and proteins. Interactions among matrix components within biofilms are responsible for creating an adaptable structure during biofilm development. Extracellular DNA, as an important matrix component in biofilms [5, 6], can be used by bacteria for several vital functions; for example, as. In Streptococcus mutans biofilms, the interaction between eDNA and glucan results in the formation of filamentous structures that play an important role in connecting bacterial cells [16]. In the case of P. aeruginosa, eDNA and the exopolysaccharide Psl physically interact in biofilms to form the web of Psl–eDNA fibres, which function as a skeleton facilitating bacterial adhesion and growth [17]. The eDNA–EPS interaction is important for the construction of biofilm architecture

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