Diverse high-torque bacterial flagellar motors assemble wider stator rings using a conserved protein scaffold

Beeby, Morgan; Ribardo, Deborah A.; Brennan, Caitlin A.; Ruby, Edward G.; Jensen, Grant J.; Hendrixson, David R.

doi:10.1073/pnas.1518952113

Cited by 180 publications

(291 citation statements)

References 71 publications

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“…Spirochete species, such as T. primitia and B. burgdorferi, have 16 putative stator units as visualized by cryo-ET (29,30). Recent data have suggested that the C. jejuni motor can possess 17 stator units while Vibrio fischeri has 13 stator units (57). Our data indicate that the H. pylori motor can assemble 18 stator units, potentially allowing for the generation of higher torque than other bacterial species.…”

Section: Discussionmentioning

confidence: 66%

Imaging the Motility and Chemotaxis Machineries in Helicobacter pylori by Cryo-Electron Tomography

et al. 2017

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Helicobacter pylori is a bacterial pathogen that can cause many gastrointestinal diseases, including ulcers and gastric cancer. A unique chemotaxis-mediated motility is critical for H. pylori to colonize in the human stomach and to establish chronic infection, but the underlying molecular mechanisms are not well understood. Here, we employ cryo-electron tomography (cryo-ET) to reveal detailed structures of the H. pylori cell envelope, including the sheathed flagella and chemotaxis arrays. Notably, H. pylori possesses a distinctive periplasmic cage-like structure with 18-fold symmetry. We propose that this structure forms a robust platform for recruiting 18 torque generators, which likely provide the higher torque needed for swimming in high-viscosity environments. We also reveal a series of key flagellar assembly intermediates, providing structural evidence that flagellar assembly is tightly coupled with the biogenesis of the membrane sheath. Finally, we determine the structure of putative chemotaxis arrays at the flagellar pole, which have implications for how the direction of flagellar rotation is regulated. Together, our pilot cryo-ET studies provide novel structural insights into the unipolar flagella of H. pylori and lay a foundation for a better understanding of the unique motility of this organism.IMPORTANCE Helicobacter pylori is a highly motile bacterial pathogen that colonizes approximately 50% of the world's population. H. pylori can move readily within the viscous mucosal layer of the stomach. It has become increasingly clear that its unique flagella-driven motility is essential for successful gastric colonization and pathogenesis. Here, we use advanced imaging techniques to visualize novel in situ structures with unprecedented detail in intact H. pylori cells. Remarkably, H. pylori possesses multiple unipolar flagella, which are driven by one of the largest flagellar motors found in bacteria. These large motors presumably provide the higher torque needed by the bacterial pathogens to navigate in the viscous environment of the human stomach.

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Section: Discussionmentioning

confidence: 66%

Imaging the Motility and Chemotaxis Machineries in Helicobacter pylori by Cryo-Electron Tomography

et al. 2017

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“…3). Altogether, these studies can be used to gain further insight into the evolution of the multiprotein complex of the flagellar motor (57).…”

Section: Expanding the Toolboxmentioning

confidence: 99%

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

et al. 2017

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The structure and function of two-component and chemotactic signaling and different aspects related to the motility of bacteria and archaea are key research areas in modern microbiology. Escherichia coli is the traditional model organism used to study chemotaxis signaling and motility. However, the recent study of a wide range of bacteria and even some archaea with different lifestyles has provided new insight into the ecophysiology of chemotaxis, which is essential for the establishment of different pathogens or beneficial bacteria in a host. The expanded range of model organisms has also permitted the study of chemosensory pathways unrelated to chemotaxis, multiple chemotaxis pathways within an organism, and new types of chemoreceptors. This research has greatly benefitted from technical advances in the field of cryomicroscopy, which continues to reveal with increasing resolution the complexity and diversity of large protein complexes like the flagellar motor or chemoreceptor arrays. In addition, sensitive instruments now allow an increasing number of experiments to be conducted at the single-cell level, thereby revealing information that is beginning to bridge the gap between individual cells and population behavior. Evidence has also accumulated showing that bacteria have evolved different mechanisms for surface sensing, which appears to be mediated by flagella and possibly type IV pili, and that the downstream signaling involves chemosensory pathways and two-component-system-based processes. Herein, we summarize the recent advances and research tendencies in this field as presented at the latest Bacterial Locomotion and Signal Transduction (BLAST XIV) conference.KEYWORDS chemotaxis, flagella, flagellar motility, signal transduction, two-component regulatory systems T he capacity to sense and respond to changes in environmental cues is an essential feature of the prokaryotic lifestyle. As a consequence, bacteria and archaea have evolved an array of different molecular mechanisms that permit the detection of signals in order to generate appropriate cellular responses. These responses are mediated primarily by one-and two-component systems, as well as chemosensory signaling pathways (1-4). Whereas the former systems mediate changes primarily at the transcriptional level, chemosensory pathways form the basis for chemotaxis, the directed movement of prokaryotes in compound gradients. The study of signaling processes is not only of fundamental interest but may also contribute to the tackling of one of the central clinical problems, which is the increasing amount of antibiotic-resistant pathogens. There is now a significant amount of data indicating that interference with signal transduction systems, motility, and chemotaxis can be an alternative strategy to weaken or block pathogens (5, 6).In

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“…Disk complex components of the C. jejunimotor have been identified using transposon screens [51,55,56]. candidates for further components of the C. jejunimotor [55].…”

Section: Motor 133mentioning

confidence: 99%

“…C. jejuni and H. hepaticus exhibit wider C-rings 123 with diameter 53 nm [40], while the W. succinogenesC-ring appears approximately ~60 nm wide in thin-124 section EM [48]. Inspection of this wider C-ring reveals an inner lobe that is elongated relative to that in 125 Salmonella, suggestive of an additional domain or protein responsible for "spacing" the C-ring wider [51]. 126…”

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confidence: 97%

“…Recent work in C. jejunihas 119 shown that the cell pole itself has a polar depression into which the hook attaches [39,40,50]. Electron cryo-120 tomography has revealed that the epsilon-proteobacterial motor is larger than the enteric motor, with a wider 121 C-ring and multiple additional 'disk complex' components in the periplasm [40,51]. The wider C-ring is 122 conserved across all epsilon-proteobacteria imaged to date.…”

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confidence: 99%

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Motility in the epsilon-proteobacteria

Beeby

2015

Current Opinion in Microbiology

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The epsilon-proteobacteria are a widespread group of flagellated bacteria frequently associated with either animal digestive tracts or hydrothermal vents, with well-studied examples in the human pathogens of Helicobacter and Campylobacter genera. Flagellated motility is important to both pathogens and hydrothermal vent members, and a number of curious differences between the epsilon-proteobacterial and enteric bacterial motility paradigms make them worthy of further study. The epsilon-proteobacteria have evolved to swim at high speed and through viscous media that immobilize enterics, a phenotype that may be accounted for by the molecular architecture of the unusually large epsilonproteobacterial flagellar motor. This review summarizes what is known about epsilon-proteobacterial motility and focuses on a number of recent discoveries that rationalize the differences with enteric flagellar motility.Motility in the epsilon-proteobacteria animal digestive tracts or hydrothermal vents, with well-studied examples in the human pathogens of 10Helicobacter and Campylobacter genera. Flagellated motility is important to both pathogens and 11 hydrothermal vent members, and a number of curious differences between the epsilon-proteobacterial and 12 enteric bacterial motility paradigms make them worthy of further study. The epsilon-proteobacteriahave 13 evolved to swim at high speed and through viscous media that immobilize enterics, a phenotype that may be 14 accounted for by the molecular architecture of the unusually large epsilon-proteobacterialflagellar motor. 15This review summarizes what is known about epsilon-proteobacterial motility and focuses on a number of 16 recent discoveries that rationalize the differences with enteric flagellar motility. 17

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Diverse high-torque bacterial flagellar motors assemble wider stator rings using a conserved protein scaffold

Cited by 180 publications

References 71 publications

Imaging the Motility and Chemotaxis Machineries in Helicobacter pylori by Cryo-Electron Tomography

Imaging the Motility and Chemotaxis Machineries in Helicobacter pylori by Cryo-Electron Tomography

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

Motility in the epsilon-proteobacteria

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