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

Abstract

Across diverse habitats, bacteria are mainly found as biofilms, surface-attached communities embedded in a self-secreted matrix of extracellular polymeric substances (EPS), which enhance bacterial recalcitrance to antimicrobial treatment and mechanical stresses. In the presence of flow and geometric constraints such as corners or constrictions, biofilms can take the form of long, suspended filaments (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 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 the production of the exopolysaccharide Pel, an important component of P. aeruginosa EPS, we reveal an concurring 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.

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.