Structure of the cyanobacterial phytochrome 2 photosensor implies a tryptophan switch for phytochrome signaling

J Biol Chem. 2013 Dec 13;288(50):35714-25. doi: 10.1074/jbc.M113.510461. Epub 2013 Oct 30.

Abstract

Phytochromes are highly versatile photoreceptors, which occur ubiquitously in plants as well as in many light-responsive microorganisms. Here, photosynthetic cyanobacteria utilize up to three different phytochrome architectures, where only the plant-like and the single-domain cyanobacteriochromes are structurally characterized so far. Cph2 represents a third group in Synechocystis species and affects their capability of phototaxis by controlling c-di-GMP synthesis and degradation. The 2.6-Å crystal structure of its red/far-red responsive photosensory module in the Pr state reveals a tandem-GAF bidomain that lacks the figure-of-eight knot of the plant/cph1 subfamily. Its covalently attached phycocyanobilin chromophore adopts a highly tilted ZZZssa conformation with a novel set of interactions between its propionates and the GAF1 domain. The tongue-like protrusion from the GAF2 domain interacts with the GAF1-bound chromophore via its conserved PRXSF, WXE, and W(G/A)G motifs. Mutagenesis showed that the integrity of the tongue is indispensable for Pr → Pfr photoconversion and involves a swap of the motifs' tryptophans within the tongue-GAF1 interface. This "Trp switch" is supposed to be a crucial element for the photochromicity of all multidomain phytochromes.

Keywords: Biliprotein; Cyanobacteria; Photochromicity; Phytochrome; Protein Conformation; Red Light Photoreceptor; Signal Transduction; Signaling; Structural Biology; c-di-GMP Signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Amino Acid Sequence
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / metabolism*
  • Binding Sites
  • Crystallography, X-Ray
  • Models, Molecular
  • Molecular Sequence Data
  • Photosynthesis
  • Phycobilins / metabolism
  • Phycocyanin / metabolism
  • Phytochrome / chemistry*
  • Phytochrome / metabolism*
  • Protein Structure, Tertiary
  • Signal Transduction*
  • Synechocystis / cytology*
  • Synechocystis / metabolism*
  • Tryptophan*

Substances

  • Bacterial Proteins
  • Cph2 protein, bacteria
  • Phycobilins
  • Phycocyanin
  • Phytochrome
  • phycocyanobilin
  • Tryptophan

Associated data

  • PDB/4BWI