Mechanism of bacterial outer membrane exchange revealed by quantitative microscopy

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 used quantitative microscopy techniques to characterize the stoichiometry of the intracellular TraAB complexes and the intercellular TraA-TraA interactions. We visualized the OME of single protein particles between cells and revealed that OME depends on the free diffusion of outer membrane (OM) contents. Based on the predicted structures, we propose a model that TraAB overcomes the repulsion between OMs by stressing the membranes and reducing the contact area, analogous to the eukaryotic soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs), which mediate plasma membrane fusion. Our working model provides a novel pathway that leads to an underlying conserved mechanism for membrane fusion that is a foundation process for multicellularity.