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

Proc Natl Acad Sci U S A. 2016 Mar 29;113(13):E1917-26. doi: 10.1073/pnas.1518952113. Epub 2016 Mar 14.

Abstract

Although it is known that diverse bacterial flagellar motors produce different torques, the mechanism underlying torque variation is unknown. To understand this difference better, we combined genetic analyses with electron cryo-tomography subtomogram averaging to determine in situ structures of flagellar motors that produce different torques, from Campylobacter and Vibrio species. For the first time, to our knowledge, our results unambiguously locate the torque-generating stator complexes and show that diverse high-torque motors use variants of an ancestrally related family of structures to scaffold incorporation of additional stator complexes at wider radii from the axial driveshaft than in the model enteric motor. We identify the protein components of these additional scaffold structures and elucidate their sequential assembly, demonstrating that they are required for stator-complex incorporation. These proteins are widespread, suggesting that different bacteria have tailored torques to specific environments by scaffolding alternative stator placement and number. Our results quantitatively account for different motor torques, complete the assignment of the locations of the major flagellar components, and provide crucial constraints for understanding mechanisms of torque generation and the evolution of multiprotein complexes.

Keywords: Campylobacter; bacterial flagellar motors; electron cryo-tomography; macromolecular evolution; torque.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Campylobacter jejuni / chemistry
  • Campylobacter jejuni / cytology
  • Campylobacter jejuni / genetics
  • Electron Microscope Tomography / methods
  • Flagella / chemistry*
  • Molecular Motor Proteins / chemistry*
  • Molecular Motor Proteins / metabolism
  • Multiprotein Complexes / chemistry
  • Multiprotein Complexes / metabolism
  • Protein Conformation
  • Salmonella / chemistry
  • Salmonella / cytology
  • Torque
  • Vibrio / chemistry
  • Vibrio / cytology

Substances

  • Bacterial Proteins
  • Molecular Motor Proteins
  • MotB protein, Bacteria
  • Multiprotein Complexes