An Empirical Test of Convergent Evolution in Rhodopsins

Mol Biol Evol. 2014 Jan;31(1):85-95. doi: 10.1093/molbev/mst171. Epub 2013 Sep 27.

Abstract

Rhodopsins are photochemically reactive membrane proteins that covalently bind retinal chromophores. Type I rhodopsins are found in both prokaryotes and eukaryotic microbes, whereas type II rhodopsins function as photoactivated G-protein coupled receptors (GPCRs) in animal vision. Both rhodopsin families share the seven transmembrane α-helix GPCR fold and a Schiff base linkage from a conserved lysine to retinal in helix G. Nevertheless, rhodopsins are widely cited as a striking example of evolutionary convergence, largely because the two families lack detectable sequence similarity and differ in many structural and mechanistic details. Convergence entails that the shared rhodopsin fold is so especially suited to photosensitive function that proteins from separate origins were selected for this architecture twice. Here we show, however, that the rhodopsin fold is not required for photosensitive activity. We engineered functional bacteriorhodopsin variants with novel folds, including radical noncircular permutations of the α-helices, circular permutations of an eight-helix construct, and retinal linkages relocated to other helices. These results contradict a key prediction of convergence and thereby provide an experimental attack on one of the most intractable problems in molecular evolution: how to establish structural homology for proteins devoid of discernible sequence similarity.

Keywords: bacteriorhodopsin; convergence; fold; homology; lysine; permutation.

Publication types

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

MeSH terms

  • Archaeal Proteins / chemistry
  • Archaeal Proteins / genetics
  • Evolution, Molecular*
  • Gene Expression
  • Halobacteriaceae / chemistry
  • Halobacteriaceae / genetics
  • Membrane Proteins / chemistry
  • Membrane Proteins / genetics*
  • Mutation
  • Protein Folding
  • Protein Structure, Secondary
  • Rhodopsin / chemistry
  • Rhodopsin / genetics*

Substances

  • Archaeal Proteins
  • Membrane Proteins
  • Rhodopsin