Energetics of Sheath Contraction in Contractile Injection Systems

Abstract

The process of protein and DNA translocation across lipid membranes is central to the function of any organism. A large class of large multicomponent organelles, such as bacteriophage tails, Type VI Secretion System, R-type pyocins, Serratia antifeeding prophage, and others, translocate their substrates using a rigid tube/contractile sheath mechanism. Functionally and structurally, these ‘contractile injection systems’ resemble a stretched spring (or sheath) wound around a non-contractile tube. The system is locked in a high-energy metastable state by a baseplate structure that plays an important role in sheath assembly and contraction triggering. Upon interaction of the baseplate with a target cell membrane, the sheath contracts and drives the tube through the cell envelope. A full atomic model of the sheath and tube in the extended and contracted state is available for R-type pyocin, one of the simplest representatives of contractile injection systems. The structure suggests that the contraction is accomplished by rigid body rearrangement of sheath subunits and that the transformation is driven by the energy stored in the extended conformation of the sheath during assembly. Other data show that the contraction starts at the baseplate and propagates through the sheath as a wave. The individual subunits’ trajectories are however unknown. We will discuss how we can derive these trajectories from energetics considerations. These finding are important for understanding the substrates that can be translocated by contractile injection systems.