Hydrogen-Bonding Interaction Regulates Photoisomerization of a Single-Bond-Rotation Locked Photoactive Yellow Protein Chromophore in Protein

J Phys Chem Lett. 2020 Apr 2;11(7):2470-2476. doi: 10.1021/acs.jpclett.0c00294. Epub 2020 Mar 13.

Abstract

We have employed the QM(CASPT2//CASSCF)/MM method to explore the excited-state isomerization and decay mechanism of a single-bond-rotation locked photoactive yellow protein (PYP) chromophore in wild-type and mutant proteins. The S1 state is a spectroscopically bright state in the Franck-Condon region. In this state, there exist two excited-state isomerization pathways separately related to the clockwise and anticlockwise rotations of the C=C bond. The clockwise path is favorable because of a small barrier of 2 kcal/mol and uses a novel bicycle-pedal unidirectional photoisomerization mechanism in which the involved two dihedral angles rotate asynchronously because of the reinforced hydrogen-bonding interaction between the chromophore and Cys69. Near the twisted S1 minimum, the chromophore hops to the S0 state via the S1/S0 conical intersection. Finally, the R52A mutation has small effects on the excited-state properties and photoisomerization of the locked PYP chromophore. The present work provides new insights for understanding the photochemistry of PYP chromophores in protein surroundings.

MeSH terms

  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / radiation effects
  • Coumaric Acids
  • Hydrogen Bonding
  • Isomerism
  • Models, Chemical
  • Mutation
  • Photochemical Processes
  • Photoreceptors, Microbial / chemistry*
  • Photoreceptors, Microbial / genetics
  • Photoreceptors, Microbial / radiation effects
  • Propionates / chemistry*
  • Propionates / radiation effects
  • Quantum Theory
  • Stereoisomerism
  • Thermodynamics

Substances

  • Bacterial Proteins
  • Coumaric Acids
  • Photoreceptors, Microbial
  • Propionates
  • photoactive yellow protein, Bacteria
  • p-coumaric acid