Novel transient cytoplasmic rings stabilize assembling bacterial flagellar motors

Mohammed Kaplan, Catherine M. Oikonomou, Cecily R. Wood, Georges Chreifi, Poorna Subramanian, Davi R. Ortega, Yi Wei Chang, Morgan Beeby, Carrie L. Shaffer, Grant J. Jensen

Research output: Contribution to journalArticlepeer-review

12 Scopus citations

Abstract

The process by which bacterial cells build their intricate flagellar motility apparatuses has long fascinated scientists. Our understanding of this process comes mainly from studies of purified flagella from two species, Escherichia coli and Salmonella enterica. Here, we used electron cryo-tomography (cryo-ET) to image the assembly of the flagellar motor in situ in diverse Proteobacteria: Hylemonella gracilis, Helicobacter pylori, Campylobacter jejuni, Pseudomonas aeruginosa, Pseudomonas fluorescens, and Shewanella oneidensis. Our results reveal the in situ structures of flagellar intermediates, beginning with the earliest flagellar type III secretion system core complex (fT3SScc) and MS-ring. In high-torque motors of Beta-, Gamma-, and Epsilon-proteobacteria, we discovered novel cytoplasmic rings that interact with the cytoplasmic torque ring formed by FliG. These rings, associated with the MS-ring, assemble very early and persist until the stators are recruited into their periplasmic ring; in their absence the stator ring does not assemble. By imaging mutants in Helicobacter pylori, we found that the fT3SScc proteins FliO and FliQ are required for the assembly of these novel cytoplasmic rings. Our results show that rather than a simple accretion of components, flagellar motor assembly is a dynamic process in which accessory components interact transiently to assist in building the complex nanomachine.

Original languageEnglish
Article numbere109523
JournalEMBO Journal
Volume41
Issue number10
DOIs
StatePublished - May 16 2022

Bibliographical note

Publisher Copyright:
© 2022 The Authors.

Keywords

  • assembly
  • bacterial flagellar motor
  • cryo-ET
  • high-torque
  • tomography

ASJC Scopus subject areas

  • General Neuroscience
  • Molecular Biology
  • General Biochemistry, Genetics and Molecular Biology
  • General Immunology and Microbiology

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