An Unusual Membrane-Protein Topology for Sensing Bilayer Thickness and Triggering Bacterial Biofilm Formation

Abstract

We propose a new topology of a bacterial membrane protein that serves to sense changes in mechanical bilayer properties and, through interactions with a potassium ion channel, to trigger biofilm formation (1). The membrane-associated protein MstX (2) from Bacillus subtilis self-inserts into lipid bilayers in such a way that its four helices lie parallel to the bilayer plane, with two helices residing in each of the two apposing lipid headgroup regions. This topology suggests a functional role of the protein as a modular entity for sensing membrane properties such as bilayer thickness and hydration, as indicated by a combination of different optical-spectroscopic techniques probing protein structure and dynamics as a function of the effective hydrophobic diameter of the membrane core. Accordingly, increasing membrane thickness or decreasing membrane hydration results in a loosening of the helical-bundle structure of MstX, which, through physical but noncovalent contacts, affects the open probability or the single-channel conductance of YugO, a hitherto uncharacterised potassium ion channel essential for biofilm formation that is encoded in the same bicistronic operon as MstX (3). Leakage of potassium ions through YugO finally initiates known signal transduction cascades that result in the derepression of a set of genes required for biofilm formation.