Mechanism of bacterial outer membrane exchange revealed by quantitative microscopy

Abstract

Kin recognition, the ability to distinguish self from nonself at the cellular level is critical to multicellular life. Myxococcus xanthus is a multicellular bacterium that cooperates among genetically-related cells and reduces exploitation by nonkin through outer membrane exchange (OME) of common goods and toxins. The polymorphic cell surface receptor called TraA and its partner protein TraB mediate kin recognition by OME, but its molecular mechanism remains unknown. Here we show that TraAB induce OME by overcoming the repulsive interaction between cells. Using quantitative microscopy techniques, we determined that TraA and TraB form complexes at a 1:1 ratio and that as few as one intercellular TraAB-TraAB dimer is sufficient to induce OME. We visualized the OME of single protein particles between cells and revealed that OME depends on the free diffusion of outer membrane (OM) contents. Our findings suggest a mechanism that shows analogies to the eukaryotic soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs), which mediate plasma membrane fusion. M. xanthus OME provides a novel pathway that leads to an underlying conserved mechanism for membrane fusion that is a foundation process for multicellularity.