Trends in Cell Biology
ReviewUsing Force to Punch Holes: Mechanics of Contractile Nanomachines
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
References (69)
Three-dimensional structure of the toxin-delivery particle antifeeding prophage of Serratia entomophila
J. Biol. Chem.
(2013)VgrG, Tae, Tle, and beyond: the versatile arsenal of Type VI secretion effectors
Trends Microbiol.
(2014)Type VI secretion and anti-host effectors
Curr. Opin. Microbiol.
(2016)The structure of the receptor-binding domain of the bacteriophage T4 short tail fibre reveals a knitted trimeric metal-binding fold
J. Mol. Biol.
(2003)TssK is a trimeric cytoplasmic protein interacting with components of both phage-like and membrane anchoring complexes of the Type VI secretion system
J. Biol. Chem.
(2013)Haemolysin coregulated protein is an exported receptor and chaperone of Type VI secretion substrates
Mol. Cell
(2013)Reassembly of the bacteriophage T4 tail from the core–baseplate and the monomeric sheath protein P18: a co-operative association process
J. Mol. Biol.
(1979)Purification, characterization and reassembly of the bacteriophage T4D tail sheath protein P18
J. Mol. Biol.
(1979)Structure of the VipA/B Type VI secretion complex suggests a contraction-state-specific recycling mechanism
Cell Rep.
(2014)Structure of the sheath of bacteriophage T4. I. Structure of the contracted sheath and polysheath
J. Mol. Biol.
(1967)
Polymerization of bacteriophage T4 tail sheath protein mutants truncated at the C-termini
J. Struct. Biol.
Tail length determination in bacteriophage T4
Virology
Structural conservation of the myoviridae phage tail sheath protein fold
Structure
Atomic structure of T6SS reveals interlaced array essential to function
Cell
Structure of the Type VI secretion system contractile sheath
Cell
Coevolution of the ATPase ClpV, the sheath proteins TssB and TssC, and the accessory protein TagJ/HsiE1 distinguishes Type VI secretion classes
J. Biol. Chem.
The molecular architecture of the bacteriophage T4 neck
J. Mol. Biol.
The X-ray crystal structure of the phage lambda tail terminator protein reveals the biologically relevant hexameric ring structure and demonstrates a conserved mechanism of tail termination among diverse long-tailed phages
J. Mol. Biol.
Sheath of bacteriophage T4. 3. Contraction mechanism deduced from partially contracted sheaths
J. Mol. Biol.
Visualization of the Serratia Type VI secretion system reveals unprovoked attacks and dynamic assembly
Cell Rep.
Molecular basis for the unique role of the AAA+ chaperone ClpV in Type VI protein secretion
J. Biol. Chem.
Cryo-EM study of the Pseudomonas bacteriophage phiKZ
Structure
Contractile tail machines of bacteriophages
Adv. Exp. Med. Biol.
Structure and function of bacteriophage T4
Future Microbiol.
Atomic structures of a bactericidal contractile nanotube in its pre- and postcontraction states
Nat. Struct. Mol. Biol.
A modified R-type bacteriocin specifically targeting Clostridium difficile prevents colonization of mice without affecting gut microbiota diversity
mBio
Studies of a pyocin. III. Biological properties of the pyocin
J. Biochem.
The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage
Mol. Microbiol.
Photorhabdus virulence cassettes confer injectable insecticidal activity against the wax moth
J. Bacteriol.
Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures
Science
A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus
Science
Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system
Proc. Natl. Acad. Sci. U. S. A.
Molecular weaponry: diverse effectors delivered by the Type VI secretion system
Cell. Microbiol.
Morphogenesis of the T4 tail and tail fibers
Virol. J.
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Coevolution-Guided Mapping of the Type VI Secretion Membrane Complex-Baseplate Interface
2023, Journal of Molecular BiologyT6SS: killing two bugs with one stone
2022, Trends in MicrobiologyCitation Excerpt :As previously documented for other T6SS peptidoglycan-targeting effectors [7], the exogenous addition of Tse4 into the cell culture is not sufficient to induce cell lysis; rather, Tse4 has to be delivered via the T6SS in a contact-dependent manner into or across the peptidoglycan layer [6]. The expanse of the T6SS tail tube (about 500 nm) and the strength of sheath contraction (about 15 000 kcal.mol–1) [8] are readily sufficient to penetrate the 30 nm width and stiffness of the Gram-positive cell wall. For comparison, contractile bacteriophages pierce the entire cell envelope, beside the fact that bacteriophage sheath lengths (about 90 nm) are much smaller than T6SS tail sheaths (about 800 nm).
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These authors contributed equally.