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Phototriggering Electron Flow through Re^I-modified Pseudomonas aeruginosa Azurins

Blanco-Rodríguez, Ana María and Di Bilio, Angel J. and Shih, Crystal and Museth, Anna Katrine and Clark, Ian P. and Towrie, Michael and Cannizzo, Andrea and Sudhamsu, Jawahar and Crane, Brian R. and Sýkora, Jan and Winkler, Jay R. and Gray, Harry B. and Záliš, Stanislav and Vlček, Antonín, Jr. (2011) Phototriggering Electron Flow through Re^I-modified Pseudomonas aeruginosa Azurins. Chemistry: a European Journal, 17 (19). pp. 5350-5361. ISSN 0947-6539. PMCID PMC3108028. doi:10.1002/chem.201002162.

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The [Re^I(CO)_3(4,7-dimethyl-1,10-phenanthroline)(histidine-124)(tryptophan-122)] complex, denoted [Re^I(dmp)(W122)], of Pseudomonas aeruginosa azurin behaves as a single photoactive unit that triggers very fast electron transfer (ET) from a distant (2 nm) Cu^I center in the protein. Analysis of time-resolved (ps–μs) IR spectroscopic and kinetics data collected on [Re^I(dmp)(W122)AzM] (in which M=Zn^(II), Cu^(II), Cu^I; Az=azurin) and position-122 tyrosine (Y), phenylalanine (F), and lysine (K) mutants, together with excited-state DFT/time-dependent (TD)DFT calculations and X-ray structural characterization, reveal the character, energetics, and dynamics of the relevant electronic states of the [Re^I(dmp)(W122)] unit and a cascade of photoinduced ET and relaxation steps in the corresponding Re–azurins. Optical population of [Re^I(imidazole-H124)(CO)_3]→dmp ^1CT states (CT=charge transfer) is followed by around 110 fs intersystem crossing and about 600 ps structural relaxation to a ^3CT state. The IR spectrum indicates a mixed Re^I(CO)_3,A→dmp/π→π^*(dmp) character for aromatic amino acids A122 (A=W, Y, F) and Re^I(CO)_3→dmp metal–ligand charge transfer (MLCT) for [Re^I(dmp)(K122)AzCu^(II)]. In a few ns, the ^3CT state of [Re^I(dmp)(W122)AzM] establishes an equilibrium with the [Re^I(dmp.^−)(W122.^+)AzM] charge-separated state, ^3CS, whereas the ^3CT state of the other Y, F, and K122 proteins decays to the ground state. In addition to this main pathway, ^3CS is populated by fs- and ps-W(indole)→Re^(II) ET from ^1CT and the initially “hot” ^3CT states, respectively. The ^3CS state undergoes a tens-of-ns dmp.^−→W122.^+ ET recombination leading to the ground state or, in the case of the Cu^I azurin, a competitively fast (≈30 ns over 1.12 nm) Cu^I→W.^+ ET, to give [Re^I(dmp.^−)(W122)AzCu^(II)]. The overall photoinduced CuI→Re(dmp) ET through [Re^I(dmp)(W122)AzCu^I] occurs over a 2 nm distance in <50 ns after excitation, with the intervening fast ^3CT–^3CS equilibrium being the principal accelerating factor. No reaction was observed for the three Y, F, and K122 analogues. Although the presence of [Re(dmp)(W122)AzCu^(II)] oligomers in solution was documented by mass spectrometry and phosphorescence anisotropy, the kinetics data do not indicate any significant interference from the intermolecular ET steps. The ground-state dmp–indole π–π interaction together with well-matched W/W.^+ and excited-state [Re^II(CO)_3(dmp.^−)]/[Re^I(CO)_3(dmp.^−)] potentials that result in very rapid electron interchange and ^3CT–^3CS energetic proximity, are the main factors responsible for the unique ET behavior of [Re^I(dmp)(W122)]-containing azurins.

Item Type:Article
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URLURL TypeDescription CentralArticle
Sýkora, Jan0000-0003-0936-9368
Winkler, Jay R.0000-0002-4453-9716
Gray, Harry B.0000-0002-7937-7876
Additional Information:© 2011 Wiley VCH Verlag GmbH&Co. KGaA, Weinheim. Received: July 28, 2010. Revised: December 12, 2010. Published online: April 5, 2011. We thank Lucie Sokolová (J.W. Goethe University, Frankfurt am Main) for measuring and interpreting the solution LILBID mass spectra. Research at Caltech was supported by the NSF Center for Chemical Innovation (Powering the Planet CHE-0802907 and CHE-0947829) and by NIH (DK019038 to HBG, JRW). The crystallographic work was supported by the NSF-CHE-0749997(BRC). The TRIR and theoretical investigations were funded by the STFC Rutherford Appleton Laboratory, CMSD 43, Queen Mary University of London, European COST D35 and ESF-DYNA programs, and Ministry of Education of the Czech Republic grants ME10124 and OC09043.
Group:CCI Solar Fuels
Funding AgencyGrant Number
Queen Mary University of LondonUNSPECIFIED
European COSTD35
Ministry of Education of the Czech RepublicME10124
Ministry of Education of the Czech RepublicOC09043
Subject Keywords: density functional calculations; electron transfer; IR spectroscopy; peptides; pi interactions
Issue or Number:19
PubMed Central ID:PMC3108028
Record Number:CaltechAUTHORS:20110526-090614868
Persistent URL:
Official Citation:Phototriggering Electron Flow through ReI-modified Pseudomonas aeruginosa Azurins (pages 5350–5361) Ana María Blanco-Rodríguez, Angel J. Di Bilio, Crystal Shih, Anna Katrine Museth, Ian P. Clark, Michael Towrie, Andrea Cannizzo, Jawahar Sudhamsu, Brian R. Crane, Jan Sýkora, Jay R. Winkler, Harry B. Gray, Stanislav Záliš and Antonín Vlček Jr. Article first published online: 5 APR 2011 | DOI: 10.1002/chem.201002162
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:23806
Deposited By: Ruth Sustaita
Deposited On:26 May 2011 18:13
Last Modified:09 Nov 2021 16:18

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