Abstract
The surfaces of many bacteria are decorated with long, exquisitely thin appendages called type IV pili (T4P), dynamic filaments that are rapidly polymerized and depolymerized from a pool of pilin subunits. Cycles of pilus extension, binding and retraction enable T4P to perform a phenomenally diverse array of functions, including twitching motility, DNA uptake and microcolony formation. On the basis of recent developments, a comprehensive understanding is emerging of the molecular architecture of the T4P machinery and the filament it builds, providing mechanistic insights into the assembly and retraction processes. Combined microbiological and biophysical approaches have revealed how T4P dynamics influence self-organization of bacteria, how bacteria respond to external stimuli to regulate T4P activity for directed movement, and the role of T4P retraction in surface sensing. In this Review, we discuss the T4P machine architecture and filament structure and present current molecular models for T4P dynamics, with a particular focus on recent insights into T4P retraction. We also discuss the functional consequences of T4P dynamics, which have important implications for bacterial lifestyle and pathogenesis.
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Acknowledgements
L.C. is supported by a Discovery Grant from the Natural Sciences and Engineering Research Council and a VPR RPEG grant from Simon Fraser University. B.M. is supported by the Deutsche Forschungsgemeinschaft through grant MA3898. K.T.F. is supported by a Vilas Associate Award from the University of Wisconsin–Madison Office of the Vice Chancellor for Research and Graduate Education.
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Nature Reviews Microbiology thanks G. Duménil and other anonymous reviewer(s) for their contribution to the peer review of this work.
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Supplementary Information
Glossary
- α1N
-
The conserved hydrophobic amino-terminal half of the extended α-helix of the major and minor pilins. α1N anchors the pilin subunits in the inner membrane before pilus assembly and anchors the pilin globular domains in the intact pilus filament.
- Subtomogram averaging
-
A method that enables low-resolution 3D imaging of intact type IV pilus machines within the bacterial envelope by selecting and averaging multiple volumes within a full tomogram (subtomograms) that each represent the same protein, revealing the electron density of individual components.
- PAS-like domain
-
The PAS domain is an α/β fold, named for the three proteins in which it was first identified. The motor ATPase amino-terminal domains bear structural similarity to the PAS domain.
- Correlated random walks
-
At short timescales, movements are directed, but at long timescales, the steps occur independent of the direction of the previous step.
- Tug of war
-
As the rate of the pilus detachment from the surface increases with force, local clustering of pili reduces detachment, and bacteria move preferentially in the direction where the pilus cluster is located.
- Microcolonies
-
Aggregates of bacteria that form on host tissues and synthetic substrates and are precursors to biofilms.
- Rupture force
-
The mean force at which the bond between type IV pili from adjacent cells ruptures.
- Swarming
-
A coordinated motility mechanism on semisolid surfaces driven by flagella.
- Range expansion assays
-
Assays in which labelled competing bacteria are mixed in liquid and inoculated onto an agar plate and subsequent microscopy enables quantification of competitors as a function of time.
- Phase variation
-
The reversible change between defined expression states of genes mediated by invertible DNA segments, changes in the stretches of homopolymeric nucleotides, short tandem repeats or other mechanisms.
- Pseudopilus
-
A short filament formed within the periplasm as part of the type II secretion system, so named because of structural and functional homologies to the type IV pilus.
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Craig, L., Forest, K.T. & Maier, B. Type IV pili: dynamics, biophysics and functional consequences. Nat Rev Microbiol 17, 429–440 (2019). https://doi.org/10.1038/s41579-019-0195-4
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DOI: https://doi.org/10.1038/s41579-019-0195-4
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