Evolutionary relationship of uptake systems for biopolymers in Escherichia coli: cross-complementation between the TonB-ExbB-ExbD and the TolA-TolQ-TolR proteins

Mol Microbiol. 1993 Apr;8(2):261-8. doi: 10.1111/j.1365-2958.1993.tb01570.x.


Escherichia coli possesses two energy-coupled import systems through which substances of low concentration and of a size too large to permit diffusion through the porins are translocated across the outer membrane. Group B colicins, ferric siderophores and vitamin B12 are taken up via the TonB-ExbB-ExbD, group A colicins via the TolA-TolQ-TolR system. Cross-complementation between the two systems was demonstrated in that tolQ tolR mutants transformed with plasmids carrying exbB exbD became sensitive to group A colicins, and exbB exbD mutants transformed with plasmid-encoded tolQ tolR became sensitive to group B colicins. TolQ-TolR interacted through TonB, and ExbB-ExbD interacted through TolA with the outer membrane receptors and colicins. Activity of ExbB ExbD via TolA was higher in cells lacking TonB, and activity of TolQ TolR via TonB was increased when TolA was missing. The very distinct TolA and TonB proteins mediate exclusive interaction with group A and group B receptors, respectively. ExbB-TolR and ExbD-TolQ mixtures showed little if any complementation of exbB exbD and tolQ tolR mutants indicating coevolution of ExbB with ExbD and TolQ with TolR. Sequence homology and mutual functional substitution of ExbB-ExbD and TolQ-TolR suggest the evolution of the two import systems from a single import system.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Biological Evolution
  • Biological Transport / genetics
  • Colicins / pharmacology
  • Escherichia coli / drug effects
  • Escherichia coli / genetics*
  • Escherichia coli / metabolism
  • Escherichia coli Proteins*
  • Ferrichrome / analogs & derivatives
  • Ferrichrome / pharmacology
  • Genes, Bacterial
  • Genetic Complementation Test
  • Membrane Proteins / genetics*
  • Membrane Proteins / metabolism
  • Recombinant Fusion Proteins / metabolism


  • Bacterial Proteins
  • Colicins
  • Escherichia coli Proteins
  • ExbB protein, E coli
  • Membrane Proteins
  • Recombinant Fusion Proteins
  • tolA protein, E coli
  • tonB protein, Bacteria
  • tonB protein, E coli
  • tolQ protein, E coli
  • tolR protein, E coli
  • exbD protein, E coli
  • Ferrichrome
  • albomycin