Multistep hopping and extracellular charge transfer in microbial redox chains.

Dissimilatory metal-reducing bacteria are microorganisms that gain energy by transferring respiratory electrons to extracellular solid-phase electron acceptors. In addition to its importance for physiology and natural environmental processes, this form of metabolism is being investigated for energy conversion and fuel production in bioelectrochemical systems, where microbes are used as biocatalysts at electrodes. One proposed strategy to accomplish this extracellular charge transfer involves forming a conductive pathway to electrodes by incorporating redox components on outer cell membranes and along extracellular appendages known as microbial nanowires within biofilms. To describe extracellular charge transfer in microbial redox chains, we employed a model based on incoherent hopping between sites in the chain and an interfacial treatment of electrochemical interactions with the surrounding electrodes. Based on this model, we calculated the current-voltage (I-V) characteristics and found the results to be in good agreement with I-V measurements across and along individual microbial nanowires produced by the bacterium Shewanella oneidensis MR-1. Based on our analysis, we propose that multistep hopping in redox chains constitutes a viable strategy for extracellular charge transfer in microbial biofilms.

[1]  Leonard M. Tender,et al.  Reply to the ‘Comment on “On electrical conductivity of microbial nanowires and biofilms”’ by N. S. Malvankar, M. T. Tuominen and D. R. Lovley, Energy Environ. Sci., 2012, 5, DOI: 10.1039/c2ee02613a , 2012 .

[2]  J. Lloyd,et al.  Secretion of Flavins by Shewanella Species and Their Role in Extracellular Electron Transfer , 2007, Applied and Environmental Microbiology.

[3]  P. Sommer-Larsen,et al.  Resonance and Environmental Fluctuation Effects in STM Currents through Large Adsorbed Molecules , 1992 .

[4]  Y. Bar-Or,et al.  ホルミジウムとアナベノプシスの生産する高分子凝集物質の性質(Applied and Environmental Microbiology,53,1987) , 1991 .

[5]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[6]  J. Gralnick,et al.  Ecology and biotechnology of the genus Shewanella. , 2007, Annual review of microbiology.

[7]  Kenneth H. Nealson,et al.  Breathing metals as a way of life: geobiology in action , 2002, Antonie van Leeuwenhoek.

[8]  D. R. Bond,et al.  Shewanella secretes flavins that mediate extracellular electron transfer , 2008, Proceedings of the National Academy of Sciences.

[9]  T. D. Yuzvinsky,et al.  Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1 , 2010, 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]  Harry B. Gray,et al.  Electron flow through metalloproteins. , 2010, Biochimica et biophysica acta.

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

[13]  G. Schatz.  The journal of physical chemistry letters , 2009 .

[14]  Grigoriy E. Pinchuk,et al.  Towards environmental systems biology of Shewanella , 2008, Nature Reviews Microbiology.

[15]  G. Schmid.  The Nature of Nanotechnology , 2010 .

[16]  P. Prasadb,et al.  Dephasing times and linewidths of optical transitions in molecular crystals. Temperature dependence of line shapes, linewidths, and frequencies of Raman active phonons in naphthalene , 1979 .

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

[18]  O. Bagasra,et al.  Proceedings of the National Academy of Sciences , 1914, Science.

[19]  P. Mitchell.  Coupling of Phosphorylation to Electron and Hydrogen Transfer by a Chemi-Osmotic type of Mechanism , 1961, Nature.

[20]  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.

[21]  A. Ranieri,et al.  The Reorganization Energy in Cytochrome c is Controlled by the Accessibility of the Heme to the Solvent , 2011 .

[22]  S. Lowen.  The Biophysical Journal , 1960, Nature.

[23]  Stefano Corni.  The reorganization energy of azurin in bulk solution and in the electrochemical scanning tunneling microscopy setup. , 2005, The journal of physical chemistry. B.

[24]  A. Troisi.  The speed limit for sequential charge hopping in molecular materials , 2011 .

[25]  D. Lovley,et al.  Novel Mode of Microbial Energy Metabolism: Organic Carbon Oxidation Coupled to Dissimilatory Reduction of Iron or Manganese , 1988, Applied and environmental microbiology.

[26]  C. Myers,et al.  Localization of cytochromes to the outer membrane of anaerobically grown Shewanella putrefaciens MR-1 , 1992, Journal of bacteriology.

[27]  Iain McCulloch,et al.  Organic Electronics , 2013, Advanced materials.

[28]  T. Mehta,et al.  Extracellular electron transfer via microbial nanowires , 2005, Nature.

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

[30]  Huan Liu,et al.  Electrochemical characterization of a single electricity-producing bacterial cell of Shewanella by using optical tweezers. , 2010, Angewandte Chemie.

[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]  T. Mehta,et al.  Outer Membrane c-Type Cytochromes Required for Fe(III) and Mn(IV) Oxide Reduction in Geobacter sulfurreducens , 2005, Applied and Environmental Microbiology.

[33]  E. Kandel,et al.  Proceedings of the National Academy of Sciences of the United States of America. Annual subject and author indexes. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[34]  D. Lovley,et al.  Humic substances as electron acceptors for microbial respiration , 1996, Nature.

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

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

[37]  Dianne K. Newman,et al.  A role for excreted quinones in extracellular electron transfer , 2000, Nature.

[38]  David N Beratan,et al.  Physical constraints on charge transport through bacterial nanowires. , 2012, Faraday discussions.

[39]  K. Nealson,et al.  Bacterial Manganese Reduction and Growth with Manganese Oxide as the Sole Electron Acceptor , 1988, Science.

[40]  Anthony Guiseppi-Elie,et al.  On the electrical conductivity of microbial nanowires and biofilms , 2011 .

[41]  Harry B Gray,et al.  Electron tunneling through proteins , 2003, Quarterly Reviews of Biophysics.

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

[43]  JOURNAL OF BACTERIOLOGY , 2006 .