Diversification of Campylobacter jejuni Flagellar C-ring composition impacts its structure and function in motility, flagellar assembly, and cellular processes

Louie D. Henderson, Teige R.S. Matthews-Palmer, Connor J. Gulbronson, Deborah A. Ribardo, Morgan Beeby, David R. Hendrixson

Research output: Contribution to journalArticlepeer-review

6 Scopus citations

Abstract

Bacterial flagella are reversible rotary motors that rotate external filaments for bacterial propulsion. Some flagellar motors have diversified by recruiting additional components that influence torque and rotation, but little is known about the possible diversification and evolution of core motor components. The mechanistic core of flagella is the cytoplasmic C ring, which functions as a rotor, directional switch, and assembly platform for the flagellar type III secretion system (fT3SS) ATPase. The C ring is composed of a ring of FliG proteins and a helical ring of surface presentation of antigen (SPOA) domains from the switch proteins FliM and one of two usually mutually exclusive paralogs, FliN or FliY. We investigated the composition, architecture, and function of the C ring of Campylobacter jejuni, which encodes FliG, FliM, and both FliY and FliN by a variety of interrogative approaches. We discovered a diversified C. jejuni C ring containing FliG, FliM, and both FliY, which functions as a classical FliN-like protein for flagellar assembly, and FliN, which has neofunctionalized into a structural role. Specific protein interactions drive the formation of a more complex heterooligomeric C. jejuni C-ring structure. We discovered that this complex C ring has additional cellular functions in polarly localizing FlhG for numerical regulation of flagellar biogenesis and spatial regulation of division. Furthermore, mutation of the C. jejuni C ring revealed a T3SS that was less dependent on its ATPase complex for assembly than were other systems. Our results highlight considerable evolved flagellar diversity that impacts motor output, biogenesis, and cellular processes in different species.

Original languageEnglish (US)
Article numbere02286-19
JournalmBio
Volume11
Issue number1
DOIs
StatePublished - Jan 1 2020

Keywords

  • C ring
  • Flagellar motor
  • FlhG
  • FliI
  • FliN
  • FliY
  • Polar flagella
  • Type III secretion

ASJC Scopus subject areas

  • Microbiology
  • Virology

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