Trends in Cell Biology
Volume 27, Issue 9, September 2017, Pages 623-632
Journal home page for Trends in Cell Biology

Review
Using Force to Punch Holes: Mechanics of Contractile Nanomachines

https://doi.org/10.1016/j.tcb.2017.05.003Get rights and content

Trends

Many bacterial nanomachines share a common ancestry and mode of action with contractile-tailed phages.

Recent advances in cryoelectron microscopy have allowed unprecedented insight into the structures of R-type pyocin and the T4 baseplate in both the pre- and post-contraction state.

Studies on the structures and dynamics of several components of the Type VI secretion system (T6SS) provide a detailed picture of T6SS’s mode of action and assembly.

These recent studies unravel a unique mechanism for the penetration of cellular membranes.

Using physical force to translocate macromolecules across a membrane has the advantage of being a universal solution independent of the properties of the target membrane. However, physically punching a stiff membrane is not a trivial task and three things are necessary for success: a sharp tip, a source of energy, and the ability to strongly bind to the target. In this review we describe the basic mechanism of membrane puncturing by contractile nanomachines with a focus on the T4 phage, R-type pyocin, and the bacterial Type VI secretion system (T6SS) based on recent studies of the structures and dynamics of their assembly.

Section snippets

Punching Holes into Membranes

With the evolution of membranes as partitions of cells and their compartments, a new challenge emerged: how can hydrophilic molecules be efficiently translocated across a barrier? Various mechanisms have evolved, including contractile nanomachines, which are effective and powerful systems for physically piercing membranes and allowing the translocation of macromolecules such as DNA or proteins. All contractile nanomachines comprise three major parts: a baseplate, a long tube with a sharp tip,

Baseplate

The complexity of contractile nanomachines is commonly located in the baseplate 15, 16. The baseplate serves as a nucleation site for polymerization of the tube and sheath and a change in structure of the baseplate triggers sheath contraction 1, 15, 17. Most of our knowledge of baseplate-like structures comes from extensive studies of bacteriophage T4, a model system for all contractile-sheath-like complexes despite enormous structural complexity. Recently, atomic-resolution maps of the T4

T6SS Membrane Complex

In T4 phage, the short tail fibers are assembled from trimeric gp12, attached to trimeric gp10, and connect the baseplate to the host cell surface by irreversibly binding to LPS [25], which is important for efficient infection of target cells 17, 19. By contrast, the T6SS baseplate is anchored to the cell envelope from the cytosolic side by associating with a membrane complex comprising TssJ, TssL, and TssM [26] (Figure 1). The details are unclear; however, the trimeric TssK interacts with both

Sheath–Tube Assembly

In all contractile tails, both tubes and sheaths are likely to be built via similar assembly pathways. Despite the low sequence similarity among tube proteins, their structures are almost identical among contractile tails (Figure 2) 3, 10, 21, 29. Tube proteins fold as β-sheet rolls flanked by a short α-helix and an extended loop. The monomers form hexameric rings that then stack head to tail with a twist to form a helical tube. The main difference among the structures of tube proteins is in

Concluding Remarks

With recent atomic models of the T4 phage baseplate and R-type pyocin tube–sheath in precontraction and post-contraction states 3, 17, we are approaching a detailed mechanistic understanding of the assembly and contraction of the most-studied contractile tails. It is reasonable to expect that atomic models of related contractile nanomachines, including those puncturing eukaryotic membranes, will become available in the near future. This will help us to understand how the systems evolved to

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