Physical constraints on charge transport through bacterial nanowires.

Extracellular appendages of the dissimilatory metal-reducing bacterium Shewanella oneidensis MR-1 were recently shown to sustain currents of 10(10) electrons per second over distances of 0.5 microns [El-Naggar et al., Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 18127]. However, the identity of the charge localizing sites and their organization along the "nanowire" remain unknown. We use theory to predict redox cofactor separation distances that would permit charge flow at rates of 10(10) electrons per second over 0.5 microns for voltage biases of < or = IV, using a steady-state analysis governed by a non-adiabatic electron transport mechanism. We find the observed currents necessitate a multi-step hopping transport mechanism, with charge localizing sites separated by less than 1 nm and reorganization energies that rival the lowest known in biology.

[1]  T. D. Yuzvinsky,et al.  Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1 , 2010, Proceedings of the National Academy of Sciences.

[2]  Derek R. Lovley,et al.  Alignment of the c-Type Cytochrome OmcS along Pili of Geobacter sulfurreducens , 2010, Applied and Environmental Microbiology.

[3]  Joseph Klafter,et al.  On mean residence and first passage times in finite one-dimensional systems , 1998 .

[4]  A. Nitzan,et al.  Electron transmission through molecules and molecular interfaces. , 2001, Annual review of physical chemistry.

[5]  J. Fredrickson,et al.  Electron transfer at the microbe–mineral interface: a grand challenge in biogeochemistry , 2008, Geobiology.

[6]  J. Onuchic,et al.  Adiabaticity and nonadiabaticity in bimolecular outer‐sphere charge transfer reactions , 1988 .

[7]  Derek R. Lovley,et al.  Microbial Electrosynthesis: Feeding Microbes Electricity To Convert Carbon Dioxide and Water to Multicarbon Extracellular Organic Compounds , 2010, mBio.

[8]  Ravindra Venkatramani,et al.  Steering electrons on moving pathways. , 2009, Accounts of chemical research.

[9]  Paul C Mills,et al.  Characterization of an electron conduit between bacteria and the extracellular environment , 2009, Proceedings of the National Academy of Sciences.

[10]  C. Chidsey,et al.  Free Energy and Temperature Dependence of Electron Transfer at the Metal-Electrolyte Interface , 1991, Science.

[11]  J. Onuchic,et al.  Protein electron transfer rates set by the bridging secondary and tertiary structure. , 1991, Science.

[12]  D. Waldeck,et al.  The Nature of Electronic Coupling between Ferrocene and Gold through Alkanethiolate Monolayers on Electrodes: The Importance of Chain Composition, Interchain Coupling, and Quantum Interference , 2001 .

[13]  David N. Beratan,et al.  Fluctuations in biological and bioinspired electron-transfer reactions. , 2010, Annual review of physical chemistry.

[14]  Harry B. Gray,et al.  Electron flow through metalloproteins. , 2010, Biochimica et biophysica acta.

[15]  K. Nealson,et al.  The molecular density of states in bacterial nanowires. , 2008, Biophysical journal.

[16]  Fraser A. Armstrong,et al.  Reaction of complex metalloproteins studied by protein-film voltammetry , 1997 .

[17]  B. Logan Exoelectrogenic bacteria that power microbial fuel cells , 2009, Nature Reviews Microbiology.

[18]  John M. Zachara,et al.  Structure of a bacterial cell surface decaheme electron conduit , 2011, Proceedings of the National Academy of Sciences.

[19]  Incoherent charge transport through molecular wires: interplay of Coulomb interaction and wire population , 2001, physics/0111069.

[20]  D. Devault,et al.  Quantum mechanical tunnelling in biological systems. , 1980, Quarterly reviews of biophysics.

[21]  J J Hopfield,et al.  Electron transfer between biological molecules by thermally activated tunneling. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Helge Lemmetyinen,et al.  An Extremely Small Reorganization Energy of Electron Transfer in Porphyrin−Fullerene Dyad , 2001 .

[23]  K. Rosso,et al.  Mechanisms of electron transfer in two decaheme cytochromes from a metal-reducing bacterium. , 2007, The journal of physical chemistry. B.

[24]  Derek R. Lovley,et al.  Biofilm and Nanowire Production Leads to Increased Current in Geobacter sulfurreducens Fuel Cells , 2006, Applied and Environmental Microbiology.

[25]  D. Richardson,et al.  Characterization of Shewanella oneidensis MtrC: a cell-surface decaheme cytochrome involved in respiratory electron transport to extracellular electron acceptors , 2007, JBIC Journal of Biological Inorganic Chemistry.

[26]  D. Beratan,et al.  Electron transfer mechanisms. , 1998, Current opinion in chemical biology.

[27]  S. Creager,et al.  Voltammetry of Redox-Active Groups Irreversibly Adsorbed onto Electrodes. Treatment Using the Marcus Relation between Rate and Overpotential , 1994 .

[28]  Jianshu Cao,et al.  Michaelis-Menten equation and detailed balance in enzymatic networks. , 2011, The journal of physical chemistry. B.

[29]  Ferdinand C. Grozema,et al.  Mechanism of charge transport in self-organizing organic materials , 2008 .

[30]  Bruce E Rittmann,et al.  Conduction‐based modeling of the biofilm anode of a microbial fuel cell , 2007, Biotechnology and bioengineering.

[31]  Alice Dohnalkova,et al.  Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Ching Leang,et al.  Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria , 2010, Science.

[33]  H. Gray,et al.  Proton-coupled electron flow in protein redox machines. , 2010, Chemical reviews.

[34]  Xiaocheng Jiang,et al.  Probing electron transfer mechanisms in Shewanella oneidensis MR-1 using a nanoelectrode platform and single-cell imaging , 2010, Proceedings of the National Academy of Sciences.

[35]  C. Wasshuber Computational Single-Electronics , 2001 .

[36]  Bruce E Cohen,et al.  Engineering of a synthetic electron conduit in living cells , 2010, Proceedings of the National Academy of Sciences.

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

[38]  R. Murray,et al.  Cyclic Voltammetric Analysis of Ferrocene Alkanethiol Monolayer Electrode Kinetics Based on Marcus Theory , 1994 .

[39]  Byoung-Chan Kim,et al.  Tunable metallic-like conductivity in microbial nanowire networks. , 2011, Nature nanotechnology.

[40]  W. Bialek,et al.  A new look at the primary charge separation in bacterial photosynthesis , 1992 .