Bioinorganic electrochemistry

Bioinorganic electrochemistry

(Parte 1 de 6)

Bioinorganic Electrochemistry Bioinorganic Electrochemistry

Bioinorganic Electrochemistry

Ole Hammerich University of Copenhagen, Denmark and

Jens Ulstrup Technical University of Denmark

Edited by

A C.I.P. Catalogue record for this book is available from the Library of Congress.

ISBN 978-1-4020-6499-9 (HB) ISBN 978-1-4020-6500-2 (e-book)

Published by Springer, P.O. Box 17, 30 A Dordrecht, The Netherlands.

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Contents

Contributing Authors vii Preface xi

1. Electron Tunneling Through Iron and Copper Proteins 1

Jay R. Winkler, Alexander R. Dunn, Corinna R. Hess, and Harry B. Gray

2. The Respiratory Enzyme as an Electrochemical Energy Transducer 25 Mårten Wikström

3. Reconstituted Redox Proteins on Surfaces for Bioelectronic Applications 37

Bilha Willner and Itamar Willner

4. Voltammetry of Adsorbed Redox Enzymes: Mechanisms in the Potential Dimension 91

Julea N. Butt and Fraser A. Armstrong

5. Electrochemistry at the DNA/Electrode Interface: New Approaches to Nucleic Acids Biosensing 129

Michael G. Hill and Shana O. Kelley vi Contents

6. Charge Transport of Solute Oligonucleotides in Metallic

Nanogaps – Observations and Some Puzzles 161 Alexander M. Kuznetsov and Jens Ulstrup

7. In Situ STM Studies of Immobilized Biomolecules at the Electrode-Electrolyte Interface 207 Richard J. Nichols, Wolfgang Haiss, David G. Fernig, Harm Van Zalinge, David J. Schiffrin, and Jens Ulstrup

8. Charge Transfer and Interfacial Bioelectrochemistry at the Nanoscale and Single-Molecule Levels 249 Jingdong Zhang, Tim Albrecht, Qijin Chi, Alexander M. Kuznetsov, and Jens Ulstrup

Index 303

Contributing Authors

Tim Albrecht Department of Chemistry and NanoDTU, Building 207, Technical University of Denmark, Kemitorvet, DK-2800 Kgs. Lyngby, Denmark

Fraser A. Armstrong Department of Chemistry, Inorganic Chemistry Laboratory, University of Oxford, Oxford, OX1 3QR, UK.

Julea N. Butt Centre for Metalloprotein Spectroscopy and Biology, School of Chemical Sciences and Pharmacy, University of East Anglia, Norwich, NR4 7TJ, UK.

Qijin Chi Department of Chemistry and NanoDTU, Building 207, Technical University of Denmark, Kemitorvet, DK-2800 Kgs. Lyngby, Denmark

Alexander R. Dunn Beckman Institute, MC 139-74, California Institute of Technology, Pasadena, California 91125, USA.

David G. Fernig The School of Biological Sciences and The Centre for Nanoscale Science, Chemistry Department, University of Liverpool, Liverpool, L69 7ZB, UK.

vii viii Contributing Authors

Harry B. Gray Beckman Institute, MC 139-74, California Institute of Technology, Pasadena, California 91125, USA.

Wolfgang Haiss Centre for Nanoscale Science, Chemistry Department, University of Liverpool, Liverpool, L69 7ZD, UK.

Corinna R. Hess Beckman Institute, MC 139-74, California Institute of Technology, Pasadena, California 91125, USA.

Michael G. Hill Occidental College, Department of Chemistry, Los Angeles, CA 90041, USA.

Shana O. Kelley Boston College, Eugene F. Merkert Chemistry Center, Chestnut Hill, MA 02467, USA.

Alexander M. Kuznetsov The A.N. Frumkin Institute of Physical Chemistry and Electrochemistry of the Russian Academy of Sciences, Leninskij Prospect 31, 119071 Moscow, Russia

Richard J. Nichols Centre for Nanoscale Science, Chemistry Department, University of Liverpool, Liverpool, L69 7ZD, UK.

David J. Schiffrin Centre for Nanoscale Science, Chemistry Department, University of Liverpool, Liverpool, L69 7ZD, UK.

Jens Ulstrup Department of Chemistry and NanoDTU, Building 207, Technical University of Denmark, Kemitorvet, DK-2800 Kgs. Lyngby, Denmark.

Mårten Wikström Helsinki Bioenergetics Group, Institute of Biotechnology, University of Helsinki, PB 65, 00014 University of Helsinki, Finland.

Bilha Willner Institute of Chemistry, The Hebrew University of Jerusalem, Jerusalem 91904, Israel.

Institute of Chemistry, The Hebrew University of Jerusalem, Jerusalem 91904, Israel.

Jay R. Winkler Beckman Institute, MC 139-74, California Institute of Technology, Pasadena, California 91125, USA.

Harm Van Zalinge Centre for Nanoscale Science, Chemistry Department, University of Liverpool, Liverpool, L69 7ZD, UK.

Jingdong Zhang Department of Chemistry and NanoDTU, Building 207, Technical University of Denmark, Kemitorvet, DK-2800 Kgs. Lyngby, Denmark.

Itamar Willner Contributing Authors

Preface

Interfacial electrochemistry of redox metalloproteins and DNA-based molecules is presently moving towards new levels of structural and functional resolution. Underlying fundamentals of electron and proton transfer are increasingly well understood although also with new challenges relating to the composite interfacial solid-electrolyte environment. The new inorganic bioelectrochemistry draws further from comprehensive studies of the interfacial environments for retaining biological charge transfer function of these highly sensitive macromolecular systems. Other biotechnology has been the use of mutant proteins, DNA-base variability and de novo synthetic metalloproteins.

Physical electrochemistry underwent a remarkable evolution from the 1970’s, almost to be likened by a renaissance and prompted by close interaction between electrochemistry and surface physics. The introduction of single-crystal atomically planar electrode surfaces was a major breakthrough and laid the foundation for other new technology such as spectroscopic techniques and statistical mechanical and electronic structure theories. Only slightly later scanning tunneling (STM) and atomic force microscopy (AFM) signalled a lift of interfacial electrochemistry to unprecedented structural resolution. Atomic resolution of pure metal and semiconductor electrode surfaces and at least sub-molecular resolution of electrochemical adsorbates could be achieved, opening new worlds of microscopic structures and processes.

Similar boundary-traversing efforts are now visible in interfacial electrochemistry of proteins and DNA-based molecules. This has led to xii Preface improved voltammetric sensitivity and structural mapping of the bioelectrochemical solid-liquid interface to single-molecule resolution. It is in fact remarkable that molecules as large and fragile as redox metalloproteins adsorbed on electrode surfaces can be mapped in their functional state by a subtle physical phenomenon, the quantum mechanical tunneling effect. These openings have offered new theoretical challenges for electron tunneling through biological macromolecules, the role of the metal centres, and the finite-size stochastic nature of the systems. Combination of protein and DNA biotechnology with electrochemistry has come to offer other perspectives in bioelectrochemical signal transfer between target molecules and external electrochemical circuitry based on strategic surface preparation and functional linker molecules.

The chapters in this volume offer overviews of electronic properties, electron transfer and electron-proton coupled charge transfer of biological molecules and macromolecules both in the natural aqueous solution environment and on metallic electrode surfaces, where the electrochemical potential controls biomolecular function. Redox metalloproteins and DNA- based molecules are primary targets, but amino acid and nucleobase building blocks are also addressed. Novel environments where proteins and DNA- based molecules are inserted in metallic nanoparticle hybrids or in situ STM configurations are other focus areas.

The chapters by Winkler et al. and by Wikström overview electron and electron-proton coupled charge transfer of both small electron transfer metalloproteins and large metalloenzyme complexes such as cyt c oxidase. A key point is the mechanistic detail now available. Percolation of electrons through the protein structure and proton hopping through conduction channels in the enzyme structures, triggered by electron transfer are important issues. Understanding of these patterns is a prerequisite for protein and enzyme voltammetry and hybrid systems for working enzyme-devices. Such perspectives are addressed by Willner and Willner, and by Butt and Armstrong. It is notable that large and fragile, sometimes multi-component enzymes can be controlled and retain close to full enzyme function at the electrochemical interface to the extent where molecular mechanisms of enzyme electrocatalysis can be mapped. This holds perspectives for multifarious technology for example in metalloenzyme biosensor function. Functional units which respond to optical, magnetic, and other signals can further be inserted between the electrode and the enzymes and biological redox chains constructed.

xiii

The chapter by Hill and Kelley addresses the interfacial electronic conductivity of DNA-based molecules controlled by the electrochemical potential. Binding of redox probes is a probe for electronic communication between the probe and the electrode through the DNA-molecular frame and therefore of the tunneling conductivity of the latter. This remains an intriguing issue as the redox-based electronic energies of the nucleobases are strongly off-resonance with the electrode Fermi energy and the redox level of the probe molecule.

Single-crystal, atomically planar electrode surfaces have paved the way for the scanning probe microscopies, STM and AFM in bioelectrochemistry. The chapter by Nichols et al. illuminates this powerful technology which has increased the structural resolution of the (bio)electrochemical electrode surfaces to sub-molecular levels. High-resolution images have been achieved for the biological building blocks, i.e. DNA nucleobases and amino acids, both of which form highly ordered monolayers on Au(1)- and Pt(1) - electrode surfaces. Dynamic surface phenomena such as adlayer phase transitions can also be followed. The image detail of individual molecules and patterns in their lateral organization holds clearly perspectives for understanding the interaction of biological liquids with solid surfaces.

The use of STM/AFM to biological macromolecules is discussed further in the chapters by Kuznetsov and Ulstrup, and by Zhang et al. Singlemolecule resolution has been achieved for both redox metalloproteins and DNA-based molecules under conditions where the molecules are active in electron transfer or enzyme function. Not only structural mapping but given adequate theoretical support, electron transfer and redox enzyme function can be addressed at the single-molecule level. The Os-complexes and the redox metalloprotein, P aeruginosa azurin discussed in chapter 8 illuminate these perspectives which extend towards ultra-sensitive biological sensors and other “device” function. STM and in situ STM are theoretically demanding because the electrical current recorded does not translate directly into molecular topography. Long-range off-resonance conductivity is broadly understood in terms of electron exchange and energy gaps of appropriate atomic or molecular orbitals with exponential distance dependence of the tunneling current expected. This is sometimes observed but weak current attenuation emerges in other cases such as for single- and double-stranded oligonucleotides. This issue presently appears unsettled.

Electronic conductivity of (bio)molecules with low-lying redox states show a quite different pattern, namely two- (or multi-)step hopping through the redox state(s) induced by environmental configurational fluctuations.

Preface xiv

Theoretical notions rest on electrochemical electron transfer but the novel environments have also disclosed new electron transfer phenomena. Switching or negative differential resistance, quite different from electrochemical electron transfer at semi-infinite electrode surfaces is immediately conspicuous. Coherent, multi-electron transfer in a single in situ STM event is another non-traditional electron transfer phenomenon.

(Bio)molecular electronics, enzyme electrochemistry, oligo-nucleotide organization, and high-resolution biological screening are exciting parts of new bioelectrochemistry. Networks of hybrid biomolecular structures are other novel targets. In a biotechnological perspective, fundamental bioelectrochemical innovation remains, however, essential. The objective of this volume is to illuminate these exciting new stages of bioinorganic electrochemistry.

Copenhagen and Lyngby, June 2007 Ole Hammerich, Jens Ulstrup

Preface

Chapter 1 ELECTRON TUNNELING THROUGH IRON

Beckman Institute, MC 139-74, California Institute of Technology, Pasadena, California 91125, USA

Iron and copper redox centers facilitate the transfer of electrons through proteins that are part of the respiratory and photosynthetic machinery of cells. Much work has been done with the goal of understanding the factors that control electron flow through these proteins.1–18 The results of many of the key experiments have been interpreted in terms of semiclassical theory.

The rate of electron transfer (ET) from a donor (D) to an acceptor (A) held at fixed distance and orientation depends on of temperature (T), reaction driving force (–ΔGo) a nuclear reorganization parameter (λ), and an electronic coupling matrix element (HAB).4,12 The reorganization parameter reflects the changes in structure and solvation that result when an electron moves from D to A. A balance between nuclear reorganization and reaction driving force determines both the transition-state configuration and the height of the barrier associated with the ET process. At the optimum driving force (–ΔGo = λ), the reaction is activationless, and the rate (kETo) is limited only by the strength of the D/A electronic coupling. When D and A are in van der Waals contact, the coupling strength is usually so large that the ET reaction is adiabatic, that is, it occurs every time the transition-state configuration is formed. In this adiabatic limit, the ET rate is independent of

HAB and the prefactor depends only on the frequency of motion along the reaction coordinate. An ET reaction is nonadiabatic when the D/A

O. Hammerich and J. Ulstrup (eds.), Bioinorganic Electrochemistry, 1–23. © 2008 Springer.

interaction is weak and the transition state must be reached many times before an electron is transferred. The electronic coupling determines the frequency of crossing from reactants (D + A) to products (D+ + A –) in the region of the transition state.

The singular feature of electron transfer is that reactions can proceed at very high rates when D and A are separated by long distances. The electron tunnels through a potential barrier between D and A; for a square barrier,

HAB displays an exponential dependence on the distance (R) between the reactants.19 The medium between redox centers potentially can control long- range ET. Owing to a 3.5–Å–1 distance-decay constant (β), the time required for electron exchange between hydrated ferrous and ferric ions is estimated to be 5×1016 years if the complexes are separated by 20 Å in a vacuum.14 Superexchange coupling via hole and electron states of the intervening medium enhances the D/A electronic interaction and produces a more gradual decrease in rate with distance. Fill the void between hydrated ferrous and ferric ions with water (β = 1.59 Å–1)20 and the time constant for 20–Å electron exchange decreases dramatically (400 years), but the reaction is still far too slow to support biological activity. If the distance decay factor for ET across a polypeptide is comparable to that found for electron tunneling across hydrocarbon bridges (β = 0.8–1.0 Å–1),14 then the time for a 20 Å electron exchange between complexed ferrous and ferric ions in the hydrophobic interior of a protein could be in the millisecond to microsecond range.

(Parte 1 de 6)

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