A kinetic perspective on extracellular electron transfer by anode-respiring bacteria.

In microbial fuel cells and electrolysis cells (MXCs), anode-respiring bacteria (ARB) oxidize organic substrates to produce electrical current. In order to develop an electrical current, ARB must transfer electrons to a solid anode through extracellular electron transfer (EET). ARB use various EET mechanisms to transfer electrons to the anode, including direct contact through outer-membrane proteins, diffusion of soluble electron shuttles, and electron transport through solid components of the extracellular biofilm matrix. In this review, we perform a novel kinetic analysis of each EET mechanism by analyzing the results available in the literature. Our goal is to evaluate how well each EET mechanism can produce a high current density (> 10 A m(-2)) without a large anode potential loss (less than a few hundred millivolts), which are feasibility goals of MXCs. Direct contact of ARB to the anode cannot achieve high current densities due to the limited number of cells that can come in direct contact with the anode. Slow diffusive flux of electron shuttles at commonly observed concentrations limits current generation and results in high potential losses, as has been observed experimentally. Only electron transport through a solid conductive matrix can explain observations of high current densities and low anode potential losses. Thus, a study of the biological components that create a solid conductive matrix is of critical importance for understanding the function of ARB.

[1]  Mauro Majone,et al.  Microbial reductive dechlorination of trichloroethene to ethene with electrodes serving as electron donors without the external addition of redox mediators , 2009, Biotechnology and bioengineering.

[2]  S. Pavlostathis,et al.  Kinetics of Anaerobic Treatment , 1991 .

[3]  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.

[4]  C. Dumas,et al.  DSA to grow electrochemically active biofilms of Geobacter sulfurreducens , 2008 .

[5]  T. Paalme,et al.  The growth rate control in Escherichia coli at near to maximum growth rates: the A-stat approach , 1997, Antonie van Leeuwenhoek.

[6]  J. Savéant,et al.  Cyclic voltammetry of immobilized redox enzymes. Interference of steady-state and non-steady-state Michaelis /Menten kinetics of the enzyme /redox cosubstrate system , 2003 .

[7]  O. Nowak,et al.  Upgrading of wastewater treatment plants equipped with rotating biological contactors to nitrification and P removal , 2000 .

[8]  B. Logan,et al.  Graphite fiber brush anodes for increased power production in air-cathode microbial fuel cells. , 2007, Environmental science & technology.

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

[10]  Perry L. McCarty,et al.  Modelling of anaerobic digestion processes (a discussion of concepts) , 1991 .

[11]  Fei Yang,et al.  A bioscrubber for hydrogen sulphide removal , 2000 .

[12]  Hanxi Yang,et al.  The direct electrocatalysis of Escherichia coli through electroactivated excretion in microbial fuel cell , 2008 .

[13]  W. Verstraete,et al.  Microbial phenazine production enhances electron transfer in biofuel cells. , 2005, Environmental science & technology.

[14]  D. G. Allen,et al.  Effect of Oxygen Partial Pressure and Chemical Oxygen Demand Loading on the Biofilm Properties in Membrane‐Aerated Bioreactors , 2009, Water environment research : a research publication of the Water Environment Federation.

[15]  K. Seeger,et al.  Semiconductor Physics: An Introduction , 1973 .

[16]  M. V. van Loosdrecht,et al.  A computational model for biofilm-based microbial fuel cells. , 2007, Water research.

[17]  V. Debabov,et al.  Electricity from microorganisms , 2008, Microbiology.

[18]  K. Weber,et al.  Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction , 2006, Nature Reviews Microbiology.

[19]  Stefano Freguia,et al.  Microbial fuel cells: methodology and technology. , 2006, Environmental science & technology.

[20]  Shweta Srikanth,et al.  Electrochemical characterization of Geobacter sulfurreducens cells immobilized on graphite paper electrodes , 2008, Biotechnology and bioengineering.

[21]  Leonard M Tender,et al.  Effect of electrode potential on electrode-reducing microbiota. , 2006, Environmental science & technology.

[22]  Washington Jose Braida Mass transfer mechanisms in air sparging systems , 1997 .

[23]  J. Moura,et al.  Electrochemical studies on c-type cytochromes at microelectrodes , 1999 .

[24]  Byung Hong Kim,et al.  A mediator-less microbial fuel cell using a metal reducing bacterium, Shewanella putrefaciens , 2002 .

[25]  Damien Feron,et al.  Catalysis of oxygen reduction in PEM fuel cell by seawater biofilm , 2005 .

[26]  Derek R Lovley,et al.  Comparison of 16S rRNA, nifD, recA, gyrB, rpoB and fusA genes within the family Geobacteraceae fam. nov. , 2004, International journal of systematic and evolutionary microbiology.

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

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

[29]  B. Glennon,et al.  Oxygen mass transfer characteristics in a membrane-aerated biofilm reactor. , 1999, Biotechnology and bioengineering.

[30]  Uwe Schröder,et al.  On the use of cyclic voltammetry for the study of anodic electron transfer in microbial fuel cells , 2008 .

[31]  Derek R. Lovley,et al.  Cyclic voltammetry of biofilms of wild type and mutant Geobacter sulfurreducens on fuel cell anodes indicates possible roles of OmcB, OmcZ, type IV pili, and protons in extracellular electron transfer , 2009 .

[32]  Hong Liu,et al.  Sustainable power generation in microbial fuel cells using bicarbonate buffer and proton transfer mechanisms. , 2008, Environmental science & technology.

[33]  B. van den Akker,et al.  Application of high rate nitrifying trickling filters for potable water treatment. , 2008, Water research.

[34]  R. C. Weast CRC Handbook of Chemistry and Physics , 1973 .

[35]  Bruce E. Rittmann,et al.  Kinetics of consumption of fermentation products by anode-respiring bacteria , 2007, Applied Microbiology and Biotechnology.

[36]  Y. Zuo,et al.  Electricity generation by Rhodopseudomonas palustris DX-1. , 2008, Environmental science & technology.

[37]  D. Lovley,et al.  Mechanisms for Accessing Insoluble Fe(III) Oxide during Dissimilatory Fe(III) Reduction by Geothrix fermentans , 2002, Applied and Environmental Microbiology.

[38]  B. Rittmann,et al.  Understanding the Distinguishing Features of a Microbial Fuel Cell as a Biomass-Based Renewable Energy Technology , 2008 .

[39]  R. Hozalski,et al.  Microbial Biofilm Voltammetry: Direct Electrochemical Characterization of Catalytic Electrode-Attached Biofilms , 2008, Applied and Environmental Microbiology.

[40]  A. Beliaev,et al.  MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR‐1 , 2001, Molecular microbiology.

[41]  Rolf U. Halden,et al.  Pre-genomic, genomic and post-genomic study of microbial communities involved in bioenergy , 2008, Nature Reviews Microbiology.

[42]  W. Verstraete,et al.  Metabolites produced by Pseudomonas sp. enable a Gram-positive bacterium to achieve extracellular electron transfer , 2008, Applied Microbiology and Biotechnology.

[43]  C. Myers,et al.  Role for Outer Membrane Cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in Reduction of Manganese Dioxide , 2001, Applied and Environmental Microbiology.

[44]  C. Léger,et al.  Direct Electrochemistry of Redox Enzymes as a Tool for Mechanistic Studies , 2008 .

[45]  H. Qian,et al.  Thermodynamics of the General Diffusion Process: Time-Reversibility and Entropy Production , 2002 .

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

[47]  D. Newman,et al.  Extracellular respiration , 2007, Molecular microbiology.

[48]  J. Monod The Growth of Bacterial Cultures , 1949 .

[49]  F. Armstrong,et al.  Diode-like behaviour of a mitochondrial electron-transport enzyme , 1992, Nature.

[50]  Kelly P. Nevin,et al.  Mechanisms for Fe(III) Oxide Reduction in Sedimentary Environments , 2002 .

[51]  Eoin Casey,et al.  Membrane-aerated biofilms for high rate biotreatment: performance appraisal, engineering principles, scale-up, and development requirements. , 2008, Environmental science & technology.

[52]  J. N. B U I S M A N,et al.  Hydrogen Production with a Microbial Biocathode , 2007 .

[53]  S. Giovannoni,et al.  Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals , 2004, Archives of Microbiology.

[54]  T. Stephenson,et al.  Pilot‐Plant Treatment of a High‐Strength Brewery Wastewater Using a Membrane‐Aeration Bioreactor , 1999 .

[55]  M. D. Rooij,et al.  Electrochemical Methods: Fundamentals and Applications , 2003 .

[56]  Willy Verstraete,et al.  Microbial ecology meets electrochemistry: electricity-driven and driving communities , 2007, The ISME Journal.

[57]  P. Mccarty,et al.  Environmental Biotechnology: Principles and Applications , 2000 .

[58]  Derek R Lovley,et al.  Graphite electrodes as electron donors for anaerobic respiration. , 2004, Environmental microbiology.

[59]  Hong Liu,et al.  Electrochemically assisted microbial production of hydrogen from acetate. , 2005, Environmental science & technology.

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

[61]  Kaichang Li,et al.  Electricity generation from polyalcohols in single-chamber microbial fuel cells. , 2008, Biosensors & bioelectronics.

[62]  Halil Hasar,et al.  Simultaneous removal of organic matter and nitrogen compounds by combining a membrane bioreactor and a membrane biofilm reactor. , 2009, Bioresource technology.

[63]  D. E. Rheinheimer,et al.  Drinking water denitrification using a membrane bioreactor. , 2004, Water research.

[64]  Prathap Parameswaran,et al.  Kinetic experiments for evaluating the Nernst-Monod model for anode-respiring bacteria (ARB) in a biofilm anode. , 2008, Environmental science & technology.

[65]  L. Tisa,et al.  Melanin Production and Use as a Soluble Electron Shuttle for Fe(III) Oxide Reduction and as a Terminal Electron Acceptor by Shewanella algae BrY , 2002, Applied and Environmental Microbiology.

[66]  Derek R. Lovley,et al.  Geobacter metallireducens accesses insoluble Fe(iii) oxide by chemotaxis , 2002, Nature.

[67]  D. Newman,et al.  Extracellular electron transfer , 2001, Cellular and Molecular Life Sciences CMLS.

[68]  W. Bae,et al.  Responses of intracellular cofactors to single and dual substrate limitations , 2000, Biotechnology and bioengineering.

[69]  J. Bockris,et al.  Fundamentals of Electrodics , 2000 .

[70]  Prathap Parameswaran,et al.  Selecting anode-respiring bacteria based on anode potential: phylogenetic, electrochemical, and microscopic characterization. , 2009, Environmental science & technology.

[71]  D. Lovley The microbe electric: conversion of organic matter to electricity. , 2008, Current opinion in biotechnology.

[72]  S. Monemian,et al.  Anaerobic treatment of synthetic medium-strength wastewater using a multistage biofilm reactor. , 2009, Bioresource technology.

[73]  B. Rittmann Opportunities for renewable bioenergy using microorganisms. , 2008, Biotechnology and bioengineering.

[74]  Thomas Joos,et al.  New frontiers in microarray technology development. , 2008, Current opinion in biotechnology.

[75]  Wei Zhang,et al.  Influence of detachment on substrate removal and microbial ecology in a heterotrophic/autotrophic biofilm. , 2007, Water research.

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

[77]  Derek R. Lovley,et al.  Evidence for Involvement of an Electron Shuttle in Electricity Generation by Geothrix fermentans , 2005, Applied and Environmental Microbiology.

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

[79]  C. H. Bamford,et al.  Electrode Kinetics: Principles and Methodology , 1986 .

[80]  Bruce E Rittmann,et al.  Proton transport inside the biofilm limits electrical current generation by anode‐respiring bacteria , 2008, Biotechnology and bioengineering.

[81]  L. Gorton,et al.  Electrochemical Study of Flavins, Phenazines, Phenoxazines and Phenothiazines Immobilized on Zirconium Phosphate , 1999 .

[82]  H. Heering,et al.  Interpreting the Catalytic Voltammetry of Electroactive Enzymes Adsorbed on Electrodes , 1998 .

[83]  Derek R. Lovley,et al.  Novel strategy for three-dimensional real-time imaging of microbial fuel cell communities: monitoring the inhibitory effects of proton accumulation within the anode biofilm , 2009 .

[84]  Abraham Esteve-Núñez,et al.  C-type cytochromes wire electricity-producing bacteria to electrodes. , 2008, Angewandte Chemie.

[85]  Andreas Kappler,et al.  Phenazines and Other Redox-Active Antibiotics Promote Microbial Mineral Reduction , 2004, Applied and Environmental Microbiology.

[86]  S. Enfors,et al.  Modeling of Overflow Metabolism in Batch and Fed‐Batch Cultures of Escherichiacoli , 1999, Biotechnology progress.

[87]  Hélène Carrère,et al.  Biofilm formation during the start-up period of an anaerobic biofilm reactor—Impact of nutrient complementation , 2006 .

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

[89]  D. Lovley,et al.  The Periplasmic 9.6-Kilodalton c-Type Cytochrome of Geobacter sulfurreducens Is Not an Electron Shuttle to Fe(III) , 1999, Journal of bacteriology.

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

[91]  L. Michaelis,et al.  POTENTIOMETRIC STUDY OF PYOCYANINE , 1931 .

[92]  Nicholas F. Gray,et al.  Biology of Wastewater Treatment , 1990 .

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

[94]  D. Lovley,et al.  Isolation, characterization and gene sequence analysis of a membrane-associated 89 kDa Fe(III) reducing cytochrome c from Geobacter sulfurreducens. , 2001, The Biochemical journal.