Structure and mechanism of the proton-driven motor that powers type 9 secretion and gliding motility

James, Rory Hennell; Deme, Justin C.; Kjær, Andreas; Alcock, Felicity; Silale, Augustinas; Lauber, Frédéric; Johnson, Steven; Berks, Ben C.; Lea, Susan M.

doi:10.1038/s41564-020-00823-6

Cited by 65 publications

(100 citation statements)

References 62 publications

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“…It is now established that the PorL/M complex uses the proton-motive force to power cargo secretion through the T9SS. The PorM rotor component of the PorL/M motor complex has a long, rotating periplasmic arm that is predicted to drive secretion (and also gliding motility in other species) via the PorK and PorN ring proteins ( 30 ). However, it is not determined whether the mechanical energy derived from the PMF is transduced to the PorK/N ring or further.…”

Section: Discussionmentioning

confidence: 99%

“…The trans-envelope complex comprises two inner membrane proteins, PorL and PorM, and two proteins associated with the OM, PorN and PorK ( 3 , 28 , 29 ). Five PorL and two PorM subunits assemble a molecular motor that uses the proton-motive force to power substrate transport ( 30 ). The PorK lipoprotein and the PorN periplasmic protein form a double-layered ring located underneath the OM and comprising 32 to 36 subunits of each protein ( 27 ).…”

Section: Introductionmentioning

confidence: 99%

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Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon

et al. 2022

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The T9SS is a newly identified protein secretion system of the Fibrobacteres - Chlorobi - Bacteroidetes superphylum used by pathogens associated with diseases of humans, fish, and poultry for the secretion and cell surface attachment of virulence factors. The T9SS comprises three known modules: (i) the trans-envelope core module comprising the PorL/M motor and the PorK/N ring, (ii) the outer membrane Sov translocon, and (iii) the cell surface attachment complex.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon

et al. 2022

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“…In order to calculate the diffusion coefficient of phages diffusing in swarm fluid of bacteria with inhibited motility, a 48-hour old culture of C. gingivalis was treated with 10 μM carbonyl cyanide-m-chlorophenylhydrazone (CCCP), an uncoupler which disrupts the proton motive force and stops T9SS driven motility 21,53 . CCCP treated C. gingivalis was used to prepare a phage-CG mix which was spotted on a TSY agar pad.…”

Section: Methodsmentioning

confidence: 99%

Bacterial swarm-mediated phage transportation disrupts a biofilm inherently protected from phage penetration

et al. 2021

Preprint

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Phage therapy, i.e., the treatment of chronic bacterial infections by virus that kill bacteria has shown promise in combating antimicrobial resistance (AMR). A typical phage particle is around 100 times bigger than a typical antibiotic molecule. Due to larger size, a phage particle diffuses slower than an antibiotic molecule, and can get trapped in the polymeric mesh of biofilm matrix. We report that a swarm of Capnocytophaga gingivalis, a bacterium abundant in the human oral microbiota, can actively transport phages over long distances. By tracking fluorescently labeled lambda phages that do not infect C. gingivalis, we demonstrate active predator transport by a C. gingivalis swarm. As a result, the rate of disruption of the prey, i.e., an Escherichia coli colony increases 10 times. Production of curli fiber by a mature E. coli biofilm blocks the intercellular space and is known to inhibit the diffusion of phages within a biofilm. We find that C. gingivalis forms tunnels within the prey biofilm. When phages are actively delivered, curli fiber containing E. coli biofilms are no longer protected against phage infection. Our results demonstrate that active delivery of the predator by a self-propelled swarm might improve the pharmacokinetics of phage therapy. This can lead to the development of a tool to combat chronic AMR biofilms.

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“…Coupling between these processes and GldM is thought to be mediated by a GldKN lipoprotein complex. b Cartoon representation of the structure of the F. johnsoniae GldLM′ complex solved previously ((11); PDB 6SY8, EMD-10893). ( Left ) Whole structure.…”

Section: Introductionmentioning

confidence: 99%

Structures of the Type IX Secretion/gliding motility motor from across the phylum Bacteroidetes

James

Deme

Hunter

et al. 2022

Preprint

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Gliding motility using cell surface adhesins and export of proteins by the Type IX Secretion System (T9SS) are two phylum-specific features of the Bacteroidetes. Both of these processes are energized by the GldLM motor complex which transduces the protonmotive force at the inner membrane into mechanical work at the outer membrane. We previously used cryo-electron microscopy to solve the structure of the GldLM motor core from Flavobacterium johnsoniae at 3.9 Å resolution (Nat Microbiol (2021) 6: 221-233). Here we present structures of homologous complexes from a range of pathogenic and environmental Bacteroidetes species at up to 3.0 Å resolution. These structures show that the architecture of the GldLM motor core is conserved across the Bacteroidetes phylum although there are species-specific differences at the N-terminus of GldL. The resolution improvements reveal a cage-like structure that ties together the membrane-proximal cytoplasmic region of GldL and influences gliding function. These findings add detail to our structural understanding of bacterial ion-driven motors that drive the T9SS and gliding motility.

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Structure and mechanism of the proton-driven motor that powers type 9 secretion and gliding motility

Cited by 65 publications

References 62 publications

Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon

Protein Interactome Analysis of the Type IX Secretion System Identifies PorW as the Missing Link between the PorK/N Ring Complex and the Sov Translocon

Bacterial swarm-mediated phage transportation disrupts a biofilm inherently protected from phage penetration

Structures of the Type IX Secretion/gliding motility motor from across the phylum Bacteroidetes

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