Energetic optimization of ion conduction rate by the K+ selectivity filter

Nature. 2001 Nov 1;414(6859):37-42. doi: 10.1038/35102000.

Abstract

The K+ selectivity filter catalyses the dehydration, transfer and rehydration of a K+ ion in about ten nanoseconds. This physical process is central to the production of electrical signals in biology. Here we show how nearly diffusion-limited rates are achieved, by analysing ion conduction and the corresponding crystallographic ion distribution in the selectivity filter of the KcsA K+ channel. Measurements with K+ and its slightly larger analogue, Rb+, lead us to conclude that the selectivity filter usually contains two K+ ions separated by one water molecule. The two ions move in a concerted fashion between two configurations, K+-water-K+-water (1,3 configuration) and water-K+-water-K+ (2,4 configuration), until a third ion enters, displacing the ion on the opposite side of the queue. For K+, the energy difference between the 1,3 and 2,4 configurations is close to zero, the condition of maximum conduction rate. The energetic balance between these configurations is a clear example of evolutionary optimization of protein function.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Bacterial Proteins*
  • Binding Sites
  • Crystallography, X-Ray
  • Diffusion
  • Electrochemistry
  • Ion Transport
  • Kinetics
  • Particle Size
  • Potassium / chemistry
  • Potassium / metabolism*
  • Potassium Channels / chemistry
  • Potassium Channels / metabolism*
  • Rubidium / chemistry
  • Rubidium / metabolism
  • Water / chemistry
  • Water / metabolism

Substances

  • Bacterial Proteins
  • Potassium Channels
  • prokaryotic potassium channel
  • Water
  • Rubidium
  • Potassium

Associated data

  • PDB/1JVM
  • PDB/1K4C
  • PDB/1K4D