Relaxation dynamics of Pseudomonas aeruginosa Re(I)(CO)3(alpha-diimine)(HisX)+ (X = 83, 107, 109, 124, 126)Cu(II) azurins.

Photoinduced relaxation processes of five structurally characterized Pseudomonas aeruginosa Re(I)(CO)(3)(alpha-diimine)(HisX) (X = 83, 107, 109, 124, 126)Cu(II) azurins have been investigated by time-resolved (ps-ns) IR spectroscopy and emission spectroscopy. Crystal structures reveal the presence of Re-azurin dimers and trimers that in two cases (X = 107, 124) involve van der Waals interactions between interdigitated diimine aromatic rings. Time-dependent emission anisotropy measurements confirm that the proteins aggregate in mM solutions (D(2)O, KP(i) buffer, pD = 7.1). Excited-state DFT calculations show that extensive charge redistribution in the Re(I)(CO)(3) --> diimine (3)MLCT state occurs: excitation of this (3)MLCT state triggers several relaxation processes in Re-azurins whose kinetics strongly depend on the location of the metallolabel on the protein surface. Relaxation is manifested by dynamic blue shifts of excited-state nu(CO) IR bands that occur with triexponential kinetics: intramolecular vibrational redistribution together with vibrational and solvent relaxation give rise to subps, approximately 2, and 8-20 ps components, while the approximately 10(2) ps kinetics are attributed to displacement (reorientation) of the Re(I)(CO)(3)(phen)(im) unit relative to the peptide chain, which optimizes Coulombic interactions of the Re(I) excited-state electron density with solvated peptide groups. Evidence also suggests that additional segmental movements of Re-bearing beta-strands occur without perturbing the reaction field or interactions with the peptide. Our work demonstrates that time-resolved IR spectroscopy and emission anisotropy of Re(I) carbonyl-diimine complexes are powerful probes of molecular dynamics at or around the surfaces of proteins and protein-protein interfacial regions.

[1]  I. Tavernelli,et al.  Combined QM/MM and classical molecular dynamics study of [Ru(bpy)3]2+ in water. , 2009, The journal of physical chemistry. B.

[2]  M. Towrie,et al.  Excited-state relaxation dynamics of Re(I) tricarbonyl complexes with macrocyclic phenanthroline ligands studied by time-resolved IR spectroscopy. , 2009, Dalton transactions.

[3]  H. Gray,et al.  Tryptophan-Accelerated Electron Flow Through Proteins , 2008, Science.

[4]  M. Chergui,et al.  Femtosecond fluorescence and intersystem crossing in rhenium(I) carbonyl-bipyridine complexes. , 2008, Journal of the American Chemical Society.

[5]  J. Sýkora,et al.  Solvation-driven excited-state dynamics of [Re(4-Et-Pyridine)(CO)3(2,2'-bipyridine)]+ in imidazolium ionic liquids. A time-resolved infrared and phosphorescence study. , 2008, The journal of physical chemistry. A.

[6]  Luyuan Zhang,et al.  Mapping hydration dynamics around a protein surface , 2007, Proceedings of the National Academy of Sciences.

[7]  M. Hargrove,et al.  Solvation dynamics in protein environments: comparison of fluorescence upconversion measurements of coumarin 153 in monomeric hemeproteins with molecular dynamics simulations. , 2007, The Journal of chemical physics.

[8]  B. Cohen,et al.  Measurement of solvation responses at multiple sites in a globular protein. , 2007, The journal of physical chemistry. B.

[9]  Joshua Jortner,et al.  Electron transfer : from isolated molecules to biomolecules , 2007 .

[10]  J. Onuchic,et al.  ELECTRON-TRANSFER TUBES , 2007 .

[11]  Korin E. Wheeler,et al.  Dynamic docking of cytochrome b5 with myoglobin and alpha-hemoglobin: heme-neutralization "squares" and the binding of electron-transfer-reactive configurations. , 2007, Journal of the American Chemical Society.

[12]  Dongping Zhong,et al.  Hydration dynamics and time scales of coupled water-protein fluctuations. , 2007, Journal of the American Chemical Society.

[13]  David N Beratan,et al.  Coupling Coherence Distinguishes Structure Sensitivity in Protein Electron Transfer , 2007, Science.

[14]  A. Vlček,et al.  Modeling of charge-transfer transitions and excited states in d6 transition metal complexes by DFT techniques , 2007 .

[15]  A. Zewail,et al.  Protein surface hydration mapped by site-specific mutations , 2006, Proceedings of the National Academy of Sciences.

[16]  P. Matousek,et al.  Excited-state dynamics of structurally characterized [ReI(CO)3(phen)(HisX)]+ (X = 83, 109) Pseudomonas aeruginosa azurins in aqueous solution. , 2006, Journal of the American Chemical Society.

[17]  Lennart Nilsson,et al.  Molecular origin of time-dependent fluorescence shifts in proteins. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[18]  P. Hamm,et al.  Solvation beyond the linear response regime. , 2005, Physical review letters.

[19]  David N Beratan,et al.  Protein dynamics and electron transfer: electronic decoherence and non-Condon effects. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Korin E. Wheeler,et al.  Differential influence of dynamic processes on forward and reverse electron transfer across a protein-protein interface. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[21]  H. Gray,et al.  Long-range electron transfer. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. Onuchic,et al.  Interprotein electron transfer from cytochrome c2 to photosynthetic reaction center: tunneling across an aqueous interface. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[23]  T. Lian,et al.  Solvation Induced Vibrational Peak Shift of a Re Bipyridyl Complex in Solution and at the Nanoporous ZrO2/Liquid Interface , 2004 .

[24]  Liang Zhao,et al.  Ultrafast hydration dynamics in protein unfolding: human serum albumin. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  P. Matousek,et al.  Excited-state dynamics of fac-[ReI(L)(CO)3(phen)]+ and fac-[ReI(L)(CO)3(5-NO2-phen)]+ (L = imidazole, 4-ethylpyridine; phen = 1,10-phenanthroline) complexes. , 2004, Inorganic chemistry.

[26]  H. Gray,et al.  Electron tunneling in rhenium-modified Pseudomonas aeruginosa azurins. , 2004, Biochimica et biophysica acta.

[27]  Samir Kumar Pal,et al.  Dynamics of water in biological recognition. , 2004, Chemical reviews.

[28]  D. Dattelbaum,et al.  Defining Electronic Excited States Using Time-Resolved Infrared Spectroscopy and Density Functional Theory Calculations† , 2004 .

[29]  D. Dattelbaum,et al.  Molecular and Electronic Structure in the Metal-to-Ligand Charge Transfer Excited States of fac-[Re(4,4‘-X2bpy)(CO)3(4-Etpy)]+* (X = CH3, H, Co2Et). Application of Density Functional Theory and Time-Resolved Infrared Spectroscopy , 2004 .

[30]  P. Matousek,et al.  Picosecond Relaxation of 3MLCT Excited States of [Re(Etpy)(CO)3(dmb)]+ and [Re(Cl)(CO)3(bpy)] as Revealed by Time-Resolved Resonance Raman, UV−vis, and IR Absorption Spectroscopy , 2004 .

[31]  Peter Hamm,et al.  Labeling vibrations by light: ultrafast transient 2D-IR spectroscopy tracks vibrational modes during photoinduced charge transfer. , 2004, Journal of the American Chemical Society.

[32]  H. Gray,et al.  Spectroscopy and reactivity of a photogenerated tryptophan radical in a structurally defined protein environment. , 2003, Journal of the American Chemical Society.

[33]  Ahmed H. Zewail,et al.  Dynamics of Water near a Protein Surface , 2003 .

[34]  Giovanni Scalmani,et al.  Energies, structures, and electronic properties of molecules in solution with the C‐PCM solvation model , 2003, J. Comput. Chem..

[35]  M. W. George,et al.  Development of a Broadband Picosecond Infrared Spectrometer and its Incorporation into an Existing Ultrafast Time-Resolved Resonance Raman, UV/Visible, and Fluorescence Spectroscopic Apparatus , 2003, Applied spectroscopy.

[36]  D. Dattelbaum,et al.  Application of time-resolved infrared spectroscopy to electronic structure in metal-to-ligand charge-transfer excited states. , 2002, Inorganic chemistry.

[37]  J. Hupp,et al.  Experimental studies of light-induced charge transfer and charge redistribution in (X(2)-bipyridine)Re(I)(CO)(3)Cl complexes. , 2002, Inorganic chemistry.

[38]  T. Lian,et al.  Time-Dependent Vibration Stokes Shift during Solvation: Experiment and Theory , 2002 .

[39]  Samir Kumar Pal,et al.  Biological water at the protein surface: Dynamical solvation probed directly with femtosecond resolution , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[40]  H. Gray,et al.  Electron tunneling in single crystals of Pseudomonas aeruginosa azurins. , 2001, Journal of the American Chemical Society.

[41]  A. Zewail,et al.  Femtosecond dynamics of a drug–protein complex: Daunomycin with Apo riboflavin-binding protein , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[42]  F. Tezcan,et al.  Electron tunneling in protein crystals , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[43]  H. Gray,et al.  Properties of photogenerated tryptophan and tyrosyl radicals in structurally characterized proteins containing rhenium(I) tricarbonyl diimines. , 2001, Journal of the American Chemical Society.

[44]  G. Crosby,et al.  Photophysical Investigations of Rhenium(I)Cl(CO)3(phenanthroline) Complexes , 2001 .

[45]  Ilya A. Balabin,et al.  Dynamically controlled protein tunneling paths in photosynthetic reaction centers. , 2000, Science.

[46]  H. Gray,et al.  Electron tunneling in biological molecules , 1999 .

[47]  G. Fleming,et al.  Solvation Dynamics in Protein Environments Studied by Photon Echo Spectroscopy , 1999 .

[48]  Vocadlo,et al.  Crystal structure, compressibility and possible phase transitions in \boldvarepsilon-FeSi studied by first-principles pseudopotential calculations. , 1999, Acta crystallographica. Section B, Structural science.

[49]  V. Barone,et al.  Toward reliable density functional methods without adjustable parameters: The PBE0 model , 1999 .

[50]  G. Loppnow,et al.  Proteins as Solvents: Blue Copper Proteins as a Molecular Ruler for Solvent Effects on Resonance Raman Intensities , 1998 .

[51]  H. Hamaguchi,et al.  Microscopic Mechanism of Solute−Solvent Energy Dissipation Probed by Picosecond Time-Resolved Raman Spectroscopy , 1997 .

[52]  Burke,et al.  Generalized Gradient Approximation Made Simple. , 1996, Physical review letters.

[53]  Ren-Jay Lin,et al.  Photophysical properties of tricarbonyl(histidine)(diimine)rhenium(I) complexes in aqueous solution , 1996 .

[54]  H. Gray,et al.  Tricarbonyl(1,10-phenanthroline) (imidazole) rhenium(I): a powerful photooxidant for investigations of electron tunneling in proteins , 1995 .

[55]  D. McRee,et al.  A visual protein crystallographic software system for X11/Xview , 1992 .

[56]  H. Stoll,et al.  Energy-adjustedab initio pseudopotentials for the second and third row transition elements , 1990 .

[57]  G. Sheldrick,et al.  SHELXL: high-resolution refinement. , 1997, Methods in enzymology.

[58]  M. W. George,et al.  Excited-state properties and reactivity of [ReCL(CO)3(2,2′-bipy)](2,2′-bipy = 2,2′-bipyridyl) studied by time-resolved infrared spectroscopy , 1993 .

[59]  J. Pople,et al.  Self‐consistent molecular orbital methods. XX. A basis set for correlated wave functions , 1980 .