Mechanism of type-III protein secretion: Regulation of FlhA conformation by a functionally critical charged-residue cluster

Mol Microbiol. 2017 Apr;104(2):234-249. doi: 10.1111/mmi.13623. Epub 2017 Feb 28.

Abstract

The bacterial flagellum contains a specialized secretion apparatus in its base that pumps certain protein subunits through the growing structure to their sites of installation beyond the membrane. A related apparatus functions in the injectisomes of gram-negative pathogens to export virulence factors into host cells. This mode of protein export is termed type-III secretion (T3S). Details of the T3S mechanism are unclear. It is energized by the proton gradient; here, a mutational approach was used to identify proton-binding groups that might function in transport. Conserved proton-binding residues in all the membrane components were tested. The results identify residues R147, R154 and D158 of FlhA as most critical. These lie in a small, well-conserved cytoplasmic domain of FlhA, located between transmembrane segments 4 and 5. Two-hybrid experiments demonstrate self-interaction of the domain, and targeted cross-linking indicates that it forms a multimeric array. A mutation that mimics protonation of the key acidic residue (D158N) was shown to trigger a global conformational change that affects the other, larger cytoplasmic domain that interacts with the export cargo. The results are discussed in the framework of a transport model based on proton-actuated movements in the cytoplasmic domains of FlhA.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism*
  • Flagella / metabolism
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism*
  • Mutation
  • Protein Conformation
  • Protein Structure, Tertiary
  • Protein Transport / physiology
  • Structure-Activity Relationship
  • Type III Secretion Systems / metabolism*
  • Type III Secretion Systems / physiology

Substances

  • Bacterial Proteins
  • FlhA protein, Bacteria
  • Membrane Proteins
  • Type III Secretion Systems