A Hybrid Secretion System Facilitates Bacterial Sporulation: A Structural Perspective

Abstract

Bacteria employ a number of dedicated secretion systems to export proteins to the extracellular environment. Several of these comprise large complexes that assemble in and around the bacterial membrane(s) to form specialized channels through which only selected proteins are actively delivered. Although typically associated with bacterial pathogenicity, a specialized variant of these secretion systems has been proposed to play a central part in bacterial sporulation, a primitive protective process that allows starving cells to form spores that survive in extreme environments. Following asymmetric division, the mother cell engulfs the forespore, leaving it surrounded by two bilayer membranes. During the engulfment process an essential channel apparatus is thought to cross both membranes to create a direct conduit between the mother cell and forespore. At least nine proteins are essential for channel formation, including SpoIIQ under forespore control and the eight SpoIIIA proteins (SpoIIIAA to -AH) under mother cell control. Presumed to form a core channel complex, several of these proteins share similarity with components of Gram-negative bacterial secretion systems, including the type II, III, and IV secretion systems and the flagellum. Based on these similarities it has been suggested that the sporulation channel represents a hybrid, secretion-like transport machinery. Recently, in-depth biochemical and structural characterization of the individual channel components accompanied by in vivo studies has further reinforced this model. Here we review and discuss these recent studies and suggest an updated model for the unique sporulation channel apparatus architecture.