Anisotropic Covalency Contributions to Superexchange Pathways in Type One Copper Active Sites

Type one (T1) Cu sites deliver electrons to catalytic Cu active sites: the mononuclear type two (T2) Cu site in nitrite reductases (NiRs) and the trinuclear Cu cluster in the multicopper oxidases (MCOs). The T1 Cu and the remote catalytic sites are connected via a Cys-His intramolecular electron-transfer (ET) bridge, which contains two potential ET pathways: P1 through the protein backbone and P2 through the H-bond between the Cys and the His. The high covalency of the T1 Cu–S(Cys) bond is shown here to activate the T1 Cu site for hole superexchange via occupied valence orbitals of the bridge. This covalency-activated electronic coupling (HDA) facilitates long-range ET through both pathways. These pathways can be selectively activated depending on the geometric and electronic structure of the T1 Cu site and thus the anisotropic covalency of the T1 Cu–S(Cys) bond. In NiRs, blue (π-type) T1 sites utilize P1 and green (σ-type) T1 sites utilize P2, with P2 being more efficient. Comparing the MCOs to NiRs, the second-sphere environment changes the conformation of the Cys-His pathway, which selectively activates HDA for superexchange by blue π sites for efficient turnover in catalysis. These studies show that a given protein bridge, here Cys-His, provides different superexchange pathways and electronic couplings depending on the anisotropic covalencies of the donor and acceptor metal sites.

[1]  Li Tian,et al.  Copper active sites in biology. , 2014, Chemical reviews.

[2]  K. Hodgson,et al.  Spectroscopic and DFT studies of second-sphere variants of the type 1 copper site in azurin: covalent and nonlocal electrostatic contributions to reduction potentials. , 2012, Journal of the American Chemical Society.

[3]  Edward I. Solomon,et al.  Recent advances in understanding blue copper proteins , 2011 .

[4]  O. Farver,et al.  Electron transfer in blue copper proteins , 2011 .

[5]  M. Ratner,et al.  Electron tunneling through sensitizer wires bound to proteins. , 2010, Coordination chemistry reviews.

[6]  E. Solomon,et al.  A variable temperature spectroscopic study on Paracoccuspantotrophus pseudoazurin: protein constraints on the blue Cu site. , 2009, Journal of inorganic biochemistry.

[7]  A. Dey,et al.  Thermodynamic equilibrium between blue and green copper sites and the role of the protein in controlling function , 2009, Proceedings of the National Academy of Sciences.

[8]  F. Armstrong,et al.  Enzymes as working or inspirational electrocatalysts for fuel cells and electrolysis. , 2008, Chemical reviews.

[9]  G. Sommer,et al.  Reference , 2008 .

[10]  M. Murphy,et al.  Effect of the methionine ligand on the reorganization energy of the type-1 copper site of nitrite reductase. , 2007, Journal of the American Chemical Society.

[11]  R. Malkin,et al.  The state and function of copper in biological systems. , 2006, Advances in enzymology and related areas of molecular biology.

[12]  E. Solomon,et al.  Spectroscopic methods in bioinorganic chemistry: blue to green to red copper sites. , 2006, Inorganic chemistry.

[13]  M. Murphy,et al.  A rearranging ligand enables allosteric control of catalytic activity in copper-containing nitrite reductase. , 2006, Journal of molecular biology.

[14]  D. Beratan,et al.  Ab initio based calculations of electron-transfer rates in metalloproteins. , 2005, The journal of physical chemistry. B.

[15]  O. Farver,et al.  Reorganization energies of the individual copper centers in dissimilatory nitrite reductases: Modulation and control of internal electron transfer , 2004 .

[16]  Scott Calabrese Barton,et al.  Enzymatic biofuel cells for implantable and microscale devices. , 2004, Chemical reviews.

[17]  G. Sawers,et al.  Met144Ala mutation of the copper‐containing nitrite reductase from Alcaligenes xylosoxidans reverses the intramolecular electron transfer , 2004, FEBS letters.

[18]  Robert K Szilagyi,et al.  Electronic structures of metal sites in proteins and models: contributions to function in blue copper proteins. , 2004, Chemical reviews.

[19]  M. Newton.  Electronic coupling in electron transfer and the influence of nuclear modes: theoretical and computational probes , 2003 .

[20]  E. Solomon,et al.  Spectroscopic studies of the Met182Thr mutant of nitrite reductase: role of the axial ligand in the geometric and electronic structure of blue and green copper sites. , 2003, Journal of the American Chemical Society.

[21]  Mark A. Ratner,et al.  Charge hopping in molecular wires as a sequence of electron-transfer reactions , 2003 .

[22]  K. Piontek,et al.  Crystal Structure of a Laccase from the FungusTrametes versicolor at 1.90-Å Resolution Containing a Full Complement of Coppers* , 2002, The Journal of Biological Chemistry.

[23]  E. Solomon,et al.  Spectroscopic Calibration of Modern Density Functional Methods Using [CuCl4]2- , 2002 .

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

[25]  Serge I. Gorelsky,et al.  Electronic structure and spectra of ruthenium diimine complexes by density functional theory and INDO/S. Comparison of the two methods , 2001 .

[26]  F. Tuczek.  Excited electronic states of transition-metal dimers and the VBCI model: an overview , 2001 .

[27]  K. Hodgson,et al.  A quantitative description of the ground-state wave function of Cu(A) by X-ray absorption spectroscopy: comparison to plastocyanin and relevance to electron transfer. , 2001, Journal of the American Chemical Society.

[28]  E. Solomon,et al.  Excited-State Exchange Coupling in Bent Mn(III)−O−Mn(III) Complexes: Dominance of the π/σ Superexchange Pathway and Its Possible Contributions to the Reactivities of Binuclear Metalloproteins , 2000 .

[29]  Gustavo L. C. Moura,et al.  Bond-Mediated Electron Tunneling in Ruthenium-Modified High-Potential Iron−Sulfur Protein , 2000 .

[30]  U. Ryde,et al.  Quantum chemical calculations of the reorganization energy of blue‐copper proteins , 1998, Protein science : a publication of the Protein Society.

[31]  Edward I. Solomon,et al.  Spectroscopic and Geometric Variations in Perturbed Blue Copper Centers: Electronic Structures of Stellacyanin and Cucumber Basic Protein , 1998 .

[32]  H. Gray,et al.  Electron transfer in ruthenium-modified plastocyanin , 1998 .

[33]  A. Winkler,et al.  Reorganization Energy of Blue Copper: Effects of Temperature and Driving Force on the Rates of Electron Transfer in Ruthenium- and Osmium-Modified Azurins , 1997 .

[34]  T. Kohzuma,et al.  Spectroscopic characterization and intramolecular electron transfer processes of native and type 2 Cu-depleted nitrite reductases , 1997, JBIC Journal of Biological Inorganic Chemistry.

[35]  Edward I. Solomon,et al.  Structural and Functional Aspects of Metal Sites in Biology. , 1996, Chemical reviews.

[36]  David Eisenberg,et al.  A missing link in cupredoxins: Crystal structure of cucumber stellacyanin at 1.6 Å resolution , 1996, Protein science : a publication of the Protein Society.

[37]  K. Hodgson,et al.  Electronic structure of the perturbed blue copper site in nitrite reductase: spectroscopic properties, bonding and implications for the entatic/rack state. , 1996 .

[38]  J. Godden,et al.  The Structure of Copper-nitrite Reductase from Achromobacter cycloclastes at Five pH Values, with NO−2 Bound and with Type II Copper Depleted (*) , 1995, The Journal of Biological Chemistry.

[39]  A. Schäfer,et al.  Fully optimized contracted Gaussian basis sets of triple zeta valence quality for atoms Li to Kr , 1994 .

[40]  E. Solomon,et al.  Copper L-edge spectral studies. A direct experimental probe of the ground-state covalency in the blue copper site in plastocyanin , 1993 .

[41]  A. Becke.  Density-functional thermochemistry. III. The role of exact exchange , 1993 .

[42]  M. Paddon-Row,et al.  Analysis of the distance dependence and magnitude of the .pi.+,.pi.- and .pi.+*,.pi.-* splittings in a series of diethynyl[n]staffanes: an ab initio molecular orbital study , 1993 .

[43]  E. Solomon,et al.  Active-site electronic structure contributions to electron-transfer pathways in rubredoxin and plastocyanin : direct versus superexchange , 1993 .

[44]  Edward I. Solomon,et al.  X-ray absorption spectroscopic studies of the blue copper site: Metal and ligand K-edge studies to probe the origin of the EPR hyperfine splitting in plastocyanin , 1993 .

[45]  H. Bartunik,et al.  Accuracy and precision in protein structure analysis: restrained least-squares refinement of the structure of poplar plastocyanin at 1.33 A resolution. , 1992, Acta crystallographica. Section B, Structural science.

[46]  E. Solomon,et al.  Axial ligand bonding in blue copper proteins , 1992 .

[47]  M. Newton,et al.  Ab initio studies of electron transfer: pathway analysis of effective transfer integrals , 1992 .

[48]  R. Huber,et al.  Crystal structure analysis of oxidized Pseudomonas aeruginosa azurin at pH 5.5 and pH 9.0. A pH-induced conformational transition involves a peptide bond flip. , 1991, Journal of molecular biology.

[49]  M. Newton,et al.  Quantum chemical probes of electron-transfer kinetics: the nature of donor-acceptor interactions , 1991 .

[50]  A. Becke,et al.  Density-functional exchange-energy approximation with correct asymptotic behavior. , 1988, Physical review. A, General physics.

[51]  Frank Jensen,et al.  A spin correction procedure for unrestricted Hartree-Fock and Møller-Plesset wavefunctions for singlet diradicals and polyradicals , 1988 .

[52]  P. Hunziker,et al.  Characterization of two allelic forms of Neurospora crassa laccase. Amino- and carboxyl-terminal processing of a precursor. , 1988, The Journal of biological chemistry.

[53]  J. Perdew,et al.  Density-functional approximation for the correlation energy of the inhomogeneous electron gas. , 1986, Physical review. B, Condensed matter.

[54]  R. Marcus,et al.  Electron transfers in chemistry and biology , 1985 .

[55]  J. Guss,et al.  Structure of oxidized poplar plastocyanin at 1.6 A resolution. , 1983, Journal of molecular biology.

[56]  E. Solomon,et al.  Spectroscopic studies on plastocyanin single crystals: a detailed electronic structure determination of the blue copper active site , 1981 .

[57]  M. Murata,et al.  X-ray crystal structure analysis of plastocyanin at 2.7 Å resolution , 1978, Nature.

[58]  Ulf Ryde,et al.  Structure, strain, and reorganization energy of blue copper models in the protein , 2001 .

[59]  E T Adman,et al.  Copper protein structures. , 1991, Advances in protein chemistry.

[60]  R. Huber,et al.  The blue oxidases, ascorbate oxidase, laccase and ceruloplasmin. Modelling and structural relationships. , 1990, European journal of biochemistry.

[61]  A. Gewirth,et al.  Electronic structure of plastocyanin: excited state spectral features , 1988 .

[62]  Stephen V. Didziulis,et al.  Variable photon energy photoelectron spectroscopic studies of copper chlorides: an experimental probe of metal-ligand bonding and changes in electronic structure on ionization , 1988 .

[63]  H. Gray.  Centenary Lecture. Long-range electron-transfer in blue copper proteins , 1986 .