Calcium-Driven Folding of RTX Domain β-Rolls Ratchets Translocation of RTX Proteins through Type I Secretion Ducts

Mol Cell. 2016 Apr 7;62(1):47-62. doi: 10.1016/j.molcel.2016.03.018.

Abstract

Calcium-binding RTX proteins are equipped with C-terminal secretion signals and translocate from the Ca(2+)-depleted cytosol of Gram-negative bacteria directly into the Ca(2+)-rich external milieu, passing through the "channel-tunnel" ducts of type I secretion systems (T1SSs). Using Bordetella pertussis adenylate cyclase toxin, we solved the structure of an essential C-terminal assembly that caps the RTX domains of RTX family leukotoxins. This is shown to scaffold directional Ca(2+)-dependent folding of the carboxy-proximal RTX repeat blocks into β-rolls. The resulting intramolecular Brownian ratchets then prevent backsliding of translocating RTX proteins in the T1SS conduits and thereby accelerate excretion of very large RTX leukotoxins from bacterial cells by a vectorial "push-ratchet" mechanism. Successive Ca(2+)-dependent and cosecretional acquisition of a functional RTX toxin structure in the course of T1SS-mediated translocation, through RTX domain folding from the C-terminal cap toward the N terminus, sets a paradigm that opens for design of virulence inhibitors of major pathogens.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenylate Cyclase Toxin / chemistry
  • Adenylate Cyclase Toxin / metabolism
  • Animals
  • Bacterial Toxins / chemistry*
  • Bacterial Toxins / metabolism*
  • Bordetella pertussis / chemistry
  • Bordetella pertussis / enzymology
  • Calcium / metabolism*
  • Cell Line
  • Gram-Negative Bacteria / chemistry
  • Gram-Negative Bacteria / metabolism*
  • Mice
  • Models, Molecular
  • Protein Folding
  • Protein Structure, Secondary
  • Protein Transport
  • Type I Secretion Systems / metabolism*

Substances

  • Adenylate Cyclase Toxin
  • Bacterial Toxins
  • Type I Secretion Systems
  • Calcium