Long-Range Charge Delocalization Mediates the Ultrafast Ligand-to-Metal Charge Transfer Dynamics at the Cu2+-Active Site in Azurin

J Phys Chem B. 2022 Jul 28;126(29):5390-5399. doi: 10.1021/acs.jpcb.2c01427. Epub 2022 Jul 7.

Abstract

The blue color in metalloprotein azurin has traditionally been attributed to the intense cysteine-to-Cu2+ ligand-to-metal charge transfer transition centered at 628 nm. Although resonance Raman measurements of the Cu2+ active site have implied that the LMCT transition electronically couples to the protein scaffold well beyond its primary metal-ligand coordination shell, the structural extent of this electronic coupling and visualization of the protein-mediated charge transfer dynamics have remained elusive. Here, using femtosecond broadband transient absorption and impulsive Raman spectroscopy, we provide direct evidence for a rapid relaxation between two distinct charge transfer states, having different spatial delocalization, within ∼300 fs followed by recombination of charges in subpicosecond time scales. We invoke the formation of a protein-centered radical cation, possibly Trp48 or a Phe residue, within 100 fs substantiating the long-range electronic coupling for the first time beyond the traditional copper active site. The Raman spectra of the excited CT state show the presence of protein-centric vibrations along with the vibrational modes assigned to the copper active site. Our results demonstrate a large delocalization length scale of the initially populated CT state, thereby highlighting the possibility of exploiting azurin photochemistry for energy conversion techniques.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Azurin* / chemistry
  • Catalytic Domain
  • Copper / chemistry
  • Ligands
  • Metalloproteins* / metabolism

Substances

  • Ligands
  • Metalloproteins
  • Azurin
  • Copper