Bifunctionality of a biofilm matrix protein controlled by redox state

Abstract

Biofilms are communities of microbial cells that are encapsulated within a self-produced polymeric matrix. The matrix is critical to the success of biofilms in diverse habitats, but despite this many details of the composition, structure, and function remain enigmatic. Biofilms formed by the Gram-positive bacterium Bacillus subtilis depend on the production of the secreted film-forming protein BslA. Here we show that a gradient of electron acceptor availability through the depth of the biofilm gives rise to two distinct functional roles for BslA and that these can be genetically separated through targeted amino acid substitutions. We establish that monomeric BslA is necessary and sufficient to give rise to complex biofilm architecture, while dimerization of BslA is required to render the community hydrophobic. Dimerization of BslA, mediated by disulfide bond formation, depends on two conserved cysteine residues located in the C-terminal region. Our findings demonstrate that bacteria have evolved multiple uses for limited elements in the matrix, allowing for alternative responses in a complex, changing environment.SignificanceThe biofilm matrix is a critical target in the hunt for novel strategies to destabilise or stabilise biofilms. Knowledge of the processes controlling matrix assembly is therefore an essential prerequisite to exploitation. Here we highlight that the complexity of the biofilm matrix is even higher than anticipated with one matrix component making two independent functional contributions to the community. The influence the protein exerts is dependent on the local environmental properties, providing another dimension to consider during analysis. These findings add to the evidence that bacteria can evolve multifunctional uses for the extracellular matrix components.

Evolution of exploitative interactions during diversification in Bacillus subtilis biofilms

“…Surface profilometry combined with wetting studies were especially helpful in the case of early morphotypes (Rough or Wrinkly): whereas they still resembled the ancestral colony in terms of macro-scale morphology, remarkable differences in microstructure and hydrophobicity were revealed. Recent work indicated that subtle differences in colony microstructure could be of profound importance for colony wetting behavior (Arnaouteli et al 2017;Werb et al 2017) and, consequently, for its resistance to antimicrobials (Arnaouteli et al 2017). To a certain extent, the measured surface complexity/hydrophobicity levels were positively correlated with the levels of matrix genes expression, .…”