Exceptionally widespread nanomachines composed of type IV pilins: the prokaryotic Swiss Army knives

Berry, Jamie-Lee; Pelicic, Vladimir

doi:10.1093/femsre/fuu001

Cited by 225 publications

(314 citation statements)

References 252 publications

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“…They are found in Gram-negative, Grampositive and archaeal organisms 6,54,55 . In archaea, these systems are responsible for the assembly of the archaeal flagellum 56 .…”

Section: Introductionmentioning

confidence: 99%

“…T4P functions vary widely and include adhesion to host cells and other surfaces, the formation of biofilms, bacterial aggregates or microcolonies, cellular invasion, electron transfer, phage and DNA uptake and twitching or gliding motility 1, 6,57 . Most T4P can dynamically elongate and retract through the action of several cytoplasmic ATPases, providing the basis for their role in bacterial motility 58,59 .…”

Section: Introductionmentioning

confidence: 99%

“…Bacterial attachment may involve contact between the bacterium and host tissues during infection, between bacteria and other surfaces or between bacteria themselves 3 . In the case of conjugative pili, bacterial contact between donor and acceptor bacteria enables the transport of DNA from one cell to another, whereas contact mediated through other types of pili may lead to infection, bacterial motility, microcolony or biofilm formation 1, [4][5][6][7] . This review will focus on the diverse structures and functions of the assembly machineries involved in the biogenesis of the five known types of pili/fimbriae in Gram-negative bacteria: the Chaperone-Usher (CU) pili, the type IV pili (T4P), the conjugative type IV secretion pili, the curli fibres, and the more recently described type V pili.…”

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confidence: 99%

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A comprehensive guide to pilus biogenesis in Gram-negative bacteria

2017

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Pili are critical virulence factors of many Gram-negative pathogens. These surface structures provide bacteria with a link to their outside environments, allowing bacteria to interact with their hosts, other surfaces or with each other. They can even provide a conduit for the exchange of information. The surface chemistries and other biophysical properties of pili are uniquely adapted to the environmental challenges faced by bacteria. The assembly of these surface structures presents a molecular engineering challenge, which bacteria have solved in a variety of unique ways. In this review, we examine recent advances in our structural understanding of various Gram-negative pilus systems and discuss their functional implications.

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“…They are found in Gram-negative, Grampositive and archaeal organisms 6,54,55 . In archaea, these systems are responsible for the assembly of the archaeal flagellum 56 .…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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A comprehensive guide to pilus biogenesis in Gram-negative bacteria

2017

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“…A large number of bacterial species are naturally competent for transformation (12). Although the genes essential for transformation are well described for various species, little is known about the molecular mechanism driving DNA import (6,13). The transformation system shares several structural and functional features with the type 4 pilus system (T4PS) and the type 2 secretion system (T2SS) (14) (Fig.…”

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confidence: 99%

Kinetics of DNA uptake during transformation provide evidence for a translocation ratchet mechanism

Hepp

Maier

2016

Proc. Natl. Acad. Sci. U.S.A.

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Horizontal gene transfer can speed up adaptive evolution and support chromosomal DNA repair. A particularly widespread mechanism of gene transfer is transformation. The initial step to transformation, namely the uptake of DNA from the environment, is supported by the type IV pilus system in most species. However, the molecular mechanism of DNA uptake remains elusive. Here, we used singlemolecule techniques for characterizing the force-dependent velocity of DNA uptake by Neisseria gonorrhoeae. We found that the DNA uptake velocity depends on the concentration of the periplasmic DNA-binding protein ComE, indicating that ComE is directly involved in the uptake process. The velocity-force relation of DNA uptake is in very good agreement with a translocation ratchet model where binding of chaperones in the periplasm biases DNA diffusion through a membrane pore in the direction of uptake. The model yields a speed of DNA uptake of 900 bp·s −1 and a reversal force of 17 pN. Moreover, by comparing the velocityforce relation of DNA uptake and type IV pilus retraction, we can exclude pilus retraction as a mechanism for DNA uptake. In conclusion, our data strongly support the model of a translocation ratchet with ComE acting as a ratcheting chaperone.

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“…Secretin pores can determine bacterial pathogenicity by their role in T4P extrusion, which is crucial for bacterial adherence and motility on solid surfaces, termed twitching motility (5)(6)(7). Natural transformation systems in bacteria, mediating the uptake of free DNA, are also dependent on secretin proteins (8,9).…”

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confidence: 99%

Topology and Structure/Function Correlation of Ring- and Gate-forming Domains in the Dynamic Secretin Complex of Thermus thermophilus

Salzer

D’Imprima

Gold

et al. 2016

Journal of Biological Chemistry

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Secretins are versatile outer membrane pores used by many bacteria to secrete proteins, toxins, or filamentous phages; extrude type IV pili (T4P); or take up DNA. Extrusion of T4P and natural transformation of DNA in the thermophilic bacterium Thermus thermophilus requires a unique secretin complex comprising six stacked rings, a membrane-embedded cone structure, and two gates that open and close a central channel. To investigate the role of distinct domains in ring and gate formation, we examined a set of deletion derivatives by cryomicroscopy techniques. Here we report that maintaining the N0 ring in the deletion derivatives led to stable PilQ complexes. Analyses of the variants unraveled that an N-terminal domain comprising a unique ␤␤␤␣␤ fold is essential for the formation of gate 2. Furthermore, we identified four ␤␣␤␤␣ domains essential for the formation of the N2 to N5 rings. Mutant studies revealed that deletion of individual ring domains significantly reduces piliation. The N1, N2, N4, and N5 deletion mutants were significantly impaired in T4P-mediated twitching motility, whereas the motility of the N3 mutant was comparable with that of wildtype cells. This indicates that the deletion of the N3 ring leads to increased pilus dynamics, thereby compensating for the reduced number of pili of the N3 mutant. All mutants exhibit a wild-type natural transformation phenotype, leading to the conclusion that DNA uptake is independent of functional T4P.

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Exceptionally widespread nanomachines composed of type IV pilins: the prokaryotic Swiss Army knives

Cited by 225 publications

References 252 publications

A comprehensive guide to pilus biogenesis in Gram-negative bacteria

A comprehensive guide to pilus biogenesis in Gram-negative bacteria

Kinetics of DNA uptake during transformation provide evidence for a translocation ratchet mechanism

Topology and Structure/Function Correlation of Ring- and Gate-forming Domains in the Dynamic Secretin Complex of Thermus thermophilus

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