Thermodynamics and Kinetics of Electron Transfer of Electrode-Immobilized Small Laccase from Streptomyces coelicolor

The thermodynamic and kinetic properties for heterogeneous electron transfer (ET) were measured for the electrode-immobilized small laccase (SLAC) from Streptomyces coelicolor subjected to different electrostatic and covalent protein-electrode linkages, using cyclic voltammetry. Once immobilized electrostatically onto a gold electrode using mixed carboxyl- and hydroxy-terminated alkane-thiolate SAMs or covalently exploiting the same SAM subjected to N-hydroxysuccinimide+1-Ethyl-3-(3-dimethylaminopropyl)carbodiimide (NHS-EDC) chemistry, the SLAC-electrode electron flow occurs through the T1 center. The E°′ values (from +0.2 to +0.1 V vs. SHE at pH 7.0) are lower by more than 0.2 V compared to the protein either in solution or immobilized with different anchoring strategies using uncharged SAMs. For the present electrostatic and covalent binding, this effect can, respectively, be ascribed to the negative charge of the SAM surfaces and to deletion of the positive charge of Lys/Arg residues due to amide bond formation which both selectively stabilize the more positively charged oxidized SLAC. Observation of enthalpy/entropy compensation within the series indicates that the immobilized proteins experience different reduction-induced solvent reorganization effects. The E°′ values for the covalently attached SLAC are sensitive to three acid base equilibria, with apparent pKa values of pKa1ox = 5.1, pKa1red = 7.5, pKa2ox = 8.4, pKa2red = 10.9, pKa2ox = 8.9, pKa2red = 11.3 possibly involving one residue close to the T1 center and two residues (Lys and/or Arg) along with moderate protein unfolding, respectively. Therefore, the E°′ value of immobilized SLAC turns out to be particularly sensitive to the anchoring mode and medium conditions.

[1]  A. Ranieri,et al.  The enthalpic and entropic terms of the reduction potential of metalloproteins: Determinants and interplay , 2021 .

[2]  A. Ranieri,et al.  Electrocatalytic Properties of Immobilized Heme Proteins: Basic Principles and Applications , 2019, ChemElectroChem.

[3]  Ping Yu,et al.  Comparative investigation of small laccase immobilized on carbon nanomaterials for direct bioelectrocatalysis of oxygen reduction , 2019, Electrochemistry Communications.

[4]  Hsien-Chang Chang,et al.  In situ study of EDC/NHS immobilization on gold surface based on attenuated total reflection surface-enhanced infrared absorption spectroscopy (ATR-SEIRAS). , 2019, Colloids and surfaces. B, Biointerfaces.

[5]  A. Díaz-Quintana,et al.  Key Role of the Local Hydrophobicity in the East Patch of Plastocyanins on Their Thermal Stability and Redox Properties , 2018, ACS omega.

[6]  R. Lontie.  Copper proteins and copper enzymes , 2018 .

[7]  Alcides J. Leguto,et al.  Tuning of Enthalpic/Entropic Parameters of a Protein Redox Center through Manipulation of the Electronic Partition Function. , 2017, Journal of the American Chemical Society.

[8]  M. Ferraroni,et al.  Structure and function of Aspergillus niger laccase McoG , 2017 .

[9]  M. McPherson,et al.  Label-free electrochemical impedance biosensor to detect human interleukin-8 in serum with sub-pg/ml sensitivity , 2016, Biosensors & bioelectronics.

[10]  Zhilei Chen,et al.  A click chemistry approach to site-specific immobilization of a small laccase enables efficient direct electron transfer in a biocathode. , 2015, Chemical communications.

[11]  V. Urlacher,et al.  Structural and redox properties of the small laccase Ssl1 from Streptomyces sviceus , 2014, The FEBS journal.

[12]  E. Ferapontova,et al.  Direct bio-electrocatalysis of O2 reduction by Streptomyces coelicolor laccase orientated at promoter-modified graphite electrodes. , 2013, Chemphyschem : a European journal of chemical physics and physical chemistry.

[13]  A. Ranieri,et al.  pH and solvent H/D isotope effects on the thermodynamics and kinetics of electron transfer for electrode-immobilized native and urea-unfolded stellacyanin. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[14]  A. Ranieri,et al.  Understanding the mechanism of short-range electron transfer using an immobilized cupredoxin. , 2012, Journal of the American Chemical Society.

[15]  Patrick Kwan,et al.  Spectroelectrochemistry of cytochrome c and azurin immobilized in nanoporous antimony-doped tin oxide. , 2011, Chemical communications.

[16]  A. Ranieri,et al.  Factors Affecting the Electron Transfer Properties of an Immobilized Cupredoxin , 2010 .

[17]  S. Sottini,et al.  Identification of a radical intermediate in the enzymatic reduction of oxygen by a small laccase. , 2009, Journal of the American Chemical Society.

[18]  A. Ranieri,et al.  Thermodynamics and kinetics of the electron transfer process of spinach plastocyanin adsorbed on a modified gold electrode , 2009 .

[19]  J. Hašek,et al.  The structure of the small laccase from Streptomyces coelicolor reveals a link between laccases and nitrite reductases. , 2009, Journal of Molecular Biology.

[20]  Scott Calabrese Barton,et al.  Bioelectrocatalytic hydrogels from electron-conducting metallopolypeptides coassembled with bifunctional enzymatic building blocks , 2008, Proceedings of the National Academy of Sciences.

[21]  P. Atanassov,et al.  Oxygen-reducing enzyme cathodes produced from SLAC, a small laccase from Streptomyces coelicolor. , 2008, Biosensors & bioelectronics.

[22]  D. Ivnitski,et al.  Electrochemical Studies of Intramolecular Electron Transfer in Laccase from Trametes versicolor , 2007 .

[23]  S. Shleev,et al.  Carbon ceramic electrodes modified with laccase from Trametes hirsuta: Fabrication, characterization and their use for phenolic compounds detection , 2007 .

[24]  F. Armstrong,et al.  A stable electrode for high-potential, electrocatalytic O(2) reduction based on rational attachment of a blue copper oxidase to a graphite surface. , 2007, Chemical communications.

[25]  F. Lisdat,et al.  Direct electrochemical conversion of bilirubin oxidase at carbon nanotube-modified glassy carbon electrodes , 2007 .

[26]  N. Devaraj,et al.  A Cytochrome c Oxidase Model Catalyzes Oxygen to Water Reduction Under Rate-Limiting Electron Flux , 2007, Science.

[27]  K. Kano,et al.  Effects of axial ligand mutation of the type I copper site in bilirubin oxidase on direct electron transfer-type bioelectrocatalytic reduction of dioxygen , 2007 .

[28]  M. Zhang,et al.  Crystal structures of E. coli laccase CueO at different copper concentrations. , 2007, Biochemical and biophysical research communications.

[29]  N. Nakamura,et al.  Direct Electron Transfer Reaction of Ascorbate Oxidase Immobilized by a Self‐Assembled Monolayer and Polymer Membrane Combined System , 2007 .

[30]  K. Kano,et al.  Bioelectrocatalytic Reduction of O2 Catalyzed by CueO from Escherichia coli Adsorbed on a Highly Oriented Pyrolytic Graphite Electrode , 2007 .

[31]  S. Shleev,et al.  Properties of native and hydrophobic laccases immobilized in the liquid-crystalline cubic phase on electrodes , 2007, JBIC Journal of Biological Inorganic Chemistry.

[32]  H. Naderi-manesh,et al.  Isolation and biochemical characterization of laccase and tyrosinase activities in a novel melanogenic soil bacterium , 2006 .

[33]  S. Shleev,et al.  Direct heterogeneous electron transfer reactions of Trametes hirsuta Laccase at bare and thiol-modified gold electrodes , 2006 .

[34]  Shaojun Dong,et al.  Facile preparation of amperometric laccase biosensor with multifunction based on the matrix of carbon nanotubes-chitosan composite. , 2006, Biosensors & bioelectronics.

[35]  P. Durão,et al.  Perturbations of the T1 copper site in the CotA laccase from Bacillus subtilis: structural, biochemical, enzymatic and stability studies , 2006, JBIC Journal of Biological Inorganic Chemistry.

[36]  R. Pierattelli,et al.  Reduction thermodynamics of the T1 Cu site in plant and fungal laccases , 2005, JBIC Journal of Biological Inorganic Chemistry.

[37]  S. Shleev,et al.  Direct electron transfer reactions of laccases from different origins on carbon electrodes. , 2005, Bioelectrochemistry.

[38]  Ulf Ryde,et al.  A combined quantum and molecular mechanical study of the O2 reductive cleavage in the catalytic cycle of multicopper oxidases. , 2005, Inorganic chemistry.

[39]  A. Ranieri,et al.  Ligand loop effects on the free energy change of redox and pH-dependent equilibria in cupredoxins probed on amicyanin variants. , 2005, Biochemistry.

[40]  Sergey Shleev,et al.  Direct electron transfer between copper-containing proteins and electrodes. , 2005, Biosensors & bioelectronics.

[41]  S. Shleev,et al.  Electrochemical redox transformations of T1 and T2 copper sites in native Trametes hirsuta laccase at gold electrode. , 2005, The Biochemical journal.

[42]  N. Go,et al.  Function and molecular evolution of multicopper blue proteins , 2005, Cellular and Molecular Life Sciences CMLS.

[43]  S. Xiao,et al.  Reactions of surface amines with heterobifunctional cross-linkers bearing both succinimidyl ester and maleimide for grafting biomolecules , 2004 .

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

[45]  S. Shleev,et al.  Direct heterogeneous electron transfer reactions of bilirubin oxidase at a spectrographic graphite electrode , 2004 .

[46]  Bart Samyn,et al.  Characterization of SLAC: A small laccase from Streptomyces coelicolor with unprecedented activity , 2004, Protein science : a publication of the Protein Society.

[47]  S. Shleev,et al.  Direct electron transfer between ligninolytic redox enzymes and electrodes , 2004 .

[48]  K. Kano,et al.  Kinetic Study of Direct Bioelectrocatalysis of Dioxygen Reduction with Bilirubin Oxidase at Carbon Electrodes , 2004 .

[49]  A. Heller.  Miniature biofuel cells , 2004 .

[50]  A. Ranieri,et al.  Enthalpy/entropy compensation phenomena in the reduction thermodynamics of electron transport metalloproteins , 2004, JBIC Journal of Biological Inorganic Chemistry.

[51]  C. Rensing,et al.  A Labile Regulatory Copper Ion Lies Near the T1 Copper Site in the Multicopper Oxidase CueO* , 2003, Journal of Biological Chemistry.

[52]  Lisandra L. Martin,et al.  Electrochemical characterization of purified Rhus vernicifera laccase: voltammetric evidence for a sequential four-electron transfer. , 2003, Biochemistry.

[53]  M. A. Carrondo,et al.  Crystal Structure of a Bacterial Endospore Coat Component , 2003, Journal of Biological Chemistry.

[54]  Kenji Kano,et al.  Glucose/O 2 Biofuel Cell Operating at Physiological Conditions , 2002 .

[55]  Manuela M. Pereira,et al.  Molecular and Biochemical Characterization of a Highly Stable Bacterial Laccase That Occurs as a Structural Component of theBacillus subtilis Endospore Coat* , 2002, The Journal of Biological Chemistry.

[56]  K. Hodgson,et al.  Nature of the intermediate formed in the reduction of O(2) to H(2)O at the trinuclear copper cluster active site in native laccase. , 2002, Journal of the American Chemical Society.

[57]  P. Hildebrandt,et al.  Electron transfer dynamics of cytochrome c bound to self-assembled monolayers on silver electrodes. , 2002, Bioelectrochemistry.

[58]  C. Rensing,et al.  CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. , 2001, Biochemical and biophysical research communications.

[59]  M. R. Tarasevich,et al.  Bioelectrocatalytic Reduction of Oxygen in the Presence of Laccase Adsorbed on Carbon Electrodes , 2001 .

[60]  W. Knoll,et al.  Dissociation of Surface Functional Groups and Preferential Adsorption of Ions on Self-Assembled Monolayers Assessed by Streaming Potential and Streaming Current Measurements , 2001 .

[61]  P. Hildebrandt,et al.  Heterogeneous Electron Transfer of Cytochrome c on Coated Silver Electrodes. Electric Field Effects on Structure and Redox Potential , 2001 .

[62]  R. Bally,et al.  Purification and characterization of the first bacterial laccase in the rhizospheric bacterium Azospirillum lipoferum , 2000 .

[63]  I. Zhulin,et al.  Laccases are widespread in bacteria. , 2000, Trends in biotechnology.

[64]  A. Ghindilis,et al.  Direct electron transfer catalysed by enzymes: application for biosensor development. , 2000, Biochemical Society transactions.

[65]  M. Sola,et al.  Redox thermodynamics of blue copper proteins , 1999 .

[66]  B. Långström,et al.  Cyclic Voltammetry and Electrocatalysis of the Blue Copper Oxidase Polyporus versicolor Laccase. , 1998 .

[67]  F. Solano,et al.  A pluripotent polyphenol oxidase from the melanogenic marine Alteromonas sp shares catalytic capabilities of tyrosinases and laccases. , 1997, Biochemical and biophysical research communications.

[68]  M. Sola,et al.  Redox thermodynamics, acid-base equilibria and salt-induced effects for the cucumber basic protein. General implications for blue-copper proteins , 1997, JBIC Journal of Biological Inorganic Chemistry.

[69]  Charles M. Lieber,et al.  Force Titrations and Ionization State Sensitive Imaging of Functional Groups in Aqueous Solutions by Chemical Force Microscopy , 1997 .

[70]  E. Solomon,et al.  Multicopper Oxidases and Oxygenases. , 1996, Chemical reviews.

[71]  G. Ullmann,et al.  Electron-Tunneling Paths in Various Electrostatic Complexes between Cytochrome c and Plastocyanin. Anisotropy of the Copper-Ligand Interactions and Dependence of the Iron-Copper Electronic Coupling on the Metalloprotein Orientation , 1995 .

[72]  A. Yaropolov,et al.  Laccase: properties, catalytic mechanism, and applicability , 1994 .

[73]  R. A. Clark,et al.  Linear-sweep voltammetry of irreversible electron transfer in surface-confined species using the marcus theory , 1994 .

[74]  Michael J. Tarlov,et al.  Characterization of cytochrome c/alkanethiolate structures prepared by self-assembly on gold , 1993 .

[75]  Harry O. Finklea,et al.  Electron-transfer kinetics in organized thiol monolayers with attached pentaammine(pyridine)ruthenium redox centers , 1992 .

[76]  A. Becka,et al.  Electrochemistry at .omega.-hydroxy thiol coated electrodes. 3. Voltage independence of the electron tunneling barrier and measurements of redox kinetics at large overpotentials , 1992 .

[77]  Michael J. Tarlov,et al.  Electron-transfer reaction of cytochrome c adsorbed on carboxylic acid terminated alkanethiol monolayer electrodes , 1991 .

[78]  H. Gray,et al.  Catalysis of the reduction of dioxygen at graphite electrodes coated with fungal laccase A , 1984 .

[79]  M. J. Weaver,et al.  Functional dependence upon ligand composition of the reaction entropies for some transition-metal redox couples containing mixed ligands , 1980 .

[80]  H. Gray,et al.  Thermodynamics of metalloprotein electron transfer reactions , 1980 .

[81]  E. Laviron.  General expression of the linear potential sweep voltammogram in the case of diffusionless electrochemical systems , 1979 .

[82]  M. J. Weaver.  Activation parameters for simple electrode reactions. Application to the elucidation of ion-solvent interactions in the transition state for heterogeneous electron transfer , 1979 .

[83]  M. J. Weaver,et al.  A survey of ligand effects upon the reaction entropies of some transition metal redox couples , 1979 .

[84]  D. Britz,et al.  iR elimination in electrochemical cells , 1978 .

[85]  H. Yoshida.  LXIII.—Chemistry of lacquer (Urushi). Part I. Communication from the Chemical Society of Tokio , 1883 .