The core signaling proteins of bacterial chemotaxis assemble to form an ultrastable complex

Biochemistry. 2009 Jul 28;48(29):6975-87. doi: 10.1021/bi900641c.

Abstract

The chemosensory pathway of bacterial chemotaxis forms a polar signaling cluster in which the fundamental signaling units, the ternary complexes, are arrayed in a highly cooperative, repeating lattice. The repeating ternary units are composed of transmembrane receptors, histidine-kinase CheA, and coupling protein CheW, but it is unknown how these three core proteins are interwoven in the assembled ultrasensitive lattice. Here, to further probe the nature of the lattice, we investigate its stability. The findings reveal that once the signaling cluster is assembled, CheA remains associated and active for days in vitro. All three core components are required for this ultrastable CheA binding and for receptor-controlled kinase activity. The stability is disrupted by low ionic strength or high pH, providing strong evidence that electrostatic repulsion between the highly acidic core components can lead to disassembly. We propose that ultrastability arises from the assembled lattice structure that establishes multiple linkages between the core components, thereby conferring thermodynamic or kinetic ultrastability to the bound state. An important, known function of the lattice structure is to facilitate receptor cooperativity, which in turn enhances pathway sensitivity. In the cell, however, the ultrastability of the lattice could lead to uncontrolled growth of the signaling complex until it fills the inner membrane. We hypothesize that such uncontrolled growth is prevented by an unidentified intracellular disassembly system that is lost when complexes are isolated from cells, thereby unmasking the intrinsic complex ultrastability. Possible biological functions of ultrastability are discussed.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Bacterial Proteins / metabolism*
  • Chemotaxis*
  • Electrophoresis, Polyacrylamide Gel
  • Hydrogen-Ion Concentration
  • Osmolar Concentration
  • Salmonella typhimurium / metabolism*
  • Signal Transduction*
  • Static Electricity

Substances

  • Bacterial Proteins