Structural elements regulating the photochromicity in a cyanobacteriochrome.

Area of Science:

• Biochemistry
• Structural Biology
• Spectroscopy

Background:

• Cyanobacteriochromes are photoreceptor proteins involved in light sensing in cyanobacteria.
• The GAF3 domain of Slr1393 contains a phycocyanobilin chromophore, responsible for light absorption.
• Understanding the structural basis of spectral shifts is crucial for deciphering photochemistry.

Purpose of the Study:

• To elucidate the three-dimensional crystal structures of the GAF3 domain of Slr1393 in different light-adapted states.
• To identify the structural determinants responsible for the spectral shift between the Pr and Pg states.
• To investigate the role of protein-chromophore interactions in regulating absorption maxima.

Main Methods:

• X-ray crystallography was used to determine the 3D structures of the GAF3 domain at high resolution (1.6–2.1 Å).
• Quantum-chemical calculations within a multiscale modeling framework were employed.
• Systematic analysis of the phycocyanobilin chromophore in the presence and absence of the protein environment.

Main Results:

• The Pr (15-Z) and Pg (15-E) states of the GAF3 domain were structurally characterized, revealing distinct chromophore conformations.
• The spectral shift is primarily attributed to the out-of-plane rotation of the chromophore's peripheral rings and helix movement.
• A third structure revealed early conformational changes during photocycle recovery, with the D-ring adopting a 15-Z configuration.

Conclusions:

• Protein-induced deviation from planarity of the phycocyanobilin chromophore's pyrrole rings is the dominant factor in spectral tuning.
• Direct electrostatic effects of the protein environment on the chromophore are negligible for spectral tuning.
• Structural insights provide a molecular basis for understanding light-induced color changes in cyanobacteriochromes.