ParP prevents dissociation of CheA from chemotactic signaling arrays and tethers them to a polar anchor

Proc Natl Acad Sci U S A. 2014 Jan 14;111(2):E255-64. doi: 10.1073/pnas.1315722111. Epub 2013 Dec 30.

Abstract

Bacterial chemotaxis proteins are organized into ordered arrays. In peritrichous organisms, such as Escherichia coli, stochastic assembly processes are thought to account for the placement of chemotaxis arrays, which are nonuniformly distributed. In contrast, we previously found that chemotactic signaling arrays in polarly flagellated vibrios are uniformly polar and that array localization is dependent on the ParA-like ATPase ParC. However, the processes that enable ParC to facilitate array localization have not been described. Here, we show that a previously uncharacterized protein, ParP, interacts with ParC and that ParP is integral to array localization in Vibrio parahaemolyticus. ParC's principal contribution to chemotaxis appears to be via positioning of ParP. Once recruited to the pole by ParC, ParP sequesters arrays at this site by capturing and preventing the dissociation of chemotactic signaling protein (CheA). Notably, ParP also stabilizes chemotactic protein complexes in the absence of ParC, indicating that some of its activity is independent of this interaction partner. ParP recruits CheA via CheA's localization and inheritance domain, a region found only in polarly flagellated organisms that encode ParP, ParC, and CheA. Thus, a tripartite (ParC-ParP-CheA) interaction network enables the polar localization and sequestration of chemotaxis arrays in polarly flagellated organisms. Localization and sequestration of chemotaxis clusters adjacent to the flagella--to which the chemotactic signal is transmitted--facilitates proper chemotaxis as well as accurate inheritance of these macromolecular machines.

Keywords: diffusion and capture; pole development; protein inheritance; protein localization; protein sequestration.

Publication types

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

MeSH terms

  • Agar
  • Bacterial Proteins / metabolism
  • Bacterial Proteins / physiology*
  • Cell Polarity / physiology*
  • Chemotaxis / physiology*
  • Computational Biology
  • DNA Topoisomerase IV / metabolism
  • Escherichia coli
  • Escherichia coli Proteins
  • Fluorescence Recovery After Photobleaching
  • Histidine Kinase
  • Membrane Proteins / metabolism
  • Methyl-Accepting Chemotaxis Proteins
  • Microscopy, Fluorescence
  • Signal Transduction / physiology*
  • Time-Lapse Imaging
  • Vibrio cholerae
  • Vibrio parahaemolyticus / genetics*
  • Vibrio parahaemolyticus / metabolism

Substances

  • Bacterial Proteins
  • Escherichia coli Proteins
  • Membrane Proteins
  • Methyl-Accepting Chemotaxis Proteins
  • Agar
  • Histidine Kinase
  • cheA protein, E coli
  • DNA Topoisomerase IV