The Functional Mechanisms and Application of Electron Shuttles in Extracellular Electron Transfer

Electron shuttles extensively exist in various environments. Some kinds of organic substances can be applied by microorganisms to produce electrons, and then the electrons can be transferred to other substances or microorganisms through electron shuttles, resulting in coexistence and interaction of diverse species of microbes. In this review, the functional mechanisms of extracellular electron transfer mediated by different electron shuttles are described. And different subtypes as well as the application of electron shuttles in microbial degradation of pollutants, microbial electricity, and the promotion of energy generation are also discussed. Summary results show that extracellular electron transfer is based on the electrogenesis microorganism with the structure of cytochromes or pili. Materials were usually used in long-distance electron transfer because of their widespread presence and abundance. Therefore, the review is beneficial to perceive the pathways of extracellular electron transfer mediated by electron shuttles and explore the contribution of different electron shuttles in extracellular electron transfer.

[1]  A. Blyth.  LVI.—The composition of cows' milk in health and disease , 1879 .

[2]  I. Fridovich,et al.  Mechanism of the antibiotic action pyocyanine , 1980, Journal of bacteriology.

[3]  M. P. Bryant,et al.  Syntrophus buswellii gen. nov., sp. nov.: a Benzoate Catabolizer from Methanogenic Ecosystems , 1984 .

[4]  J. Gregory Zeikus,et al.  Control of Interspecies Electron Flow during Anaerobic Digestion: Significance of Formate Transfer versus Hydrogen Transfer during Syntrophic Methanogenesis in Flocs , 1988, Applied and environmental microbiology.

[5]  D. Boone,et al.  Diffusion of the Interspecies Electron Carriers H2 and Formate in Methanogenic Ecosystems and Its Implications in the Measurement of Km for H2 or Formate Uptake , 1989, Applied and environmental microbiology.

[6]  D. Hassett,et al.  Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase , 1992, Infection and immunity.

[7]  B. Ahring,et al.  Interspecies Electron Transfer during Propionate and Butyrate Degradation in Mesophilic, Granular Sludge , 1995, Applied and environmental microbiology.

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

[9]  Christof Holliger,et al.  Reductive dechlorination in the energy metabolism of anaerobic bacteria , 1998 .

[10]  D. Lovley,et al.  Quinone Moieties Act as Electron Acceptors in the Reduction of Humic Substances by Humics-Reducing Microorganisms , 1998 .

[11]  H. Naveau,et al.  Anaerobic Dechlorinating Bacteria , 1998, Biotechnology progress.

[12]  S. Hashsham,et al.  Enhanced Biotransformation of Carbon Tetrachloride by Acetobacterium woodii upon Addition of Hydroxocobalamin and Fructose , 1999, Applied and Environmental Microbiology.

[13]  Y. Kamagata,et al.  Involvement of formate as an interspecies electron carrier in a syntrophic acetate-oxidizing anaerobic microorganism in coculture with methanogens. , 2001, Journal of bioscience and bioengineering.

[14]  R. Chakraborty,et al.  Diversity and Ubiquity of Bacteria Capable of Utilizing Humic Substances as Electron Donors for Anaerobic Respiration , 2002, Applied and Environmental Microbiology.

[15]  W. Verstraete,et al.  Biofuel Cells Select for Microbial Consortia That Self-Mediate Electron Transfer , 2004, Applied and Environmental Microbiology.

[16]  D. Hassett,et al.  Pseudomonas aeruginosa Pyocyanin Is Critical for Lung Infection in Mice , 2004, Infection and Immunity.

[17]  R. S. Wolfe,et al.  Methanobacillus omelianskii, a symbiotic association of two species of bacteria , 2004, Archiv für Mikrobiologie.

[18]  D. Hassett,et al.  The role of pyocyanin in Pseudomonas aeruginosa infection. , 2004, Trends in molecular medicine.

[19]  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.

[20]  Santiago Villaverde,et al.  Combined anaerobic-aerobic treatment of azo dyes--a short review of bioreactor studies. , 2005, Water research.

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

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

[23]  J. Dolfing,et al.  Exocellular electron transfer in anaerobic microbial communities. , 2006, Environmental microbiology.

[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]  Derek R Lovley,et al.  Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. , 2006, Environmental microbiology.

[26]  M. Surette,et al.  Communication in bacteria: an ecological and evolutionary perspective , 2006, Nature Reviews Microbiology.

[27]  Laurie N. DiDonato,et al.  Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens , 2007, BMC Microbiology.

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

[29]  D. Lovley,et al.  Evidence that OmcB and OmpB of Geobacter sulfurreducens are outer membrane surface proteins. , 2007, FEMS microbiology letters.

[30]  V. Orphan,et al.  Methyl sulfides as intermediates in the anaerobic oxidation of methane. , 2007, Environmental microbiology.

[31]  C. Blodau,et al.  Electron accepting capacity of dissolved organic matter as determined by reaction with metallic zinc , 2009 .

[32]  Kazuya Watanabe,et al.  Electron shuttles in biotechnology. , 2009, Current opinion in biotechnology.

[33]  Byoung-Chan Kim,et al.  Anode Biofilm Transcriptomics Reveals Outer Surface Components Essential for High Density Current Production in Geobacter sulfurreducens Fuel Cells , 2009, PloS one.

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

[35]  D. Lovley,et al.  Purification and Characterization of OmcZ, an Outer-Surface, Octaheme c-Type Cytochrome Essential for Optimal Current Production by Geobacter sulfurreducens , 2010, Applied and Environmental Microbiology.

[36]  L. Rohlin,et al.  The genome of Syntrophomonas wolfei: new insights into syntrophic metabolism and biohydrogen production. , 2010, Environmental microbiology.

[37]  S. Freguia,et al.  Flavins contained in yeast extract are exploited for anodic electron transfer by Lactococcus lactis. , 2010, Bioelectrochemistry.

[38]  R. Schwarzenbach,et al.  Novel electrochemical approach to assess the redox properties of humic substances. , 2010, Environmental science & technology.

[39]  Huifang Xu,et al.  Extracellular electron transfer through microbial reduction of solid-phase humic substances , 2010 .

[40]  N. Duke,et al.  Structural characterization of a family of cytochromes c(7) involved in Fe(III) respiration by Geobacter sulfurreducens. , 2010, Biochimica et biophysica acta.

[41]  René P Schwarzenbach,et al.  Electrochemical analysis of proton and electron transfer equilibria of the reducible moieties in humic acids. , 2011, Environmental science & technology.

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

[43]  T. Arakawa,et al.  Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe(III) reduction in Geobacter sulfurreducens. , 2011, Biochimica et biophysica acta.

[44]  Ganesh Dattatraya Saratale,et al.  Bacterial decolorization and degradation of azo dyes: a review. , 2011 .

[45]  Derek R Lovley,et al.  Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens. , 2011, Bioelectrochemistry.

[46]  Shungui Zhou,et al.  A rapid and simple electrochemical method for evaluating the electron transfer capacities of dissolved organic matter , 2011 .

[47]  Jeffrey A. Gralnick,et al.  Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella , 2011, Applied Microbiology and Biotechnology.

[48]  A. Katayama,et al.  Humin as an electron mediator for microbial reductive dehalogenation. , 2012, Environmental science & technology.

[49]  J. Jayapriya,et al.  Use of non-native phenazines to improve the performance of Pseudomonas aeruginosa MTCC 2474 catalysed fuel cells. , 2012, Bioresource technology.

[50]  D. Lovley.  Long-range electron transport to Fe(III) oxide via pili with metallic-like conductivity. , 2012, Biochemical Society transactions.

[51]  Electron transfer between periplasmic formate dehydrogenase and cytochromes c in Desulfovibrio desulfuricans ATCC 27774 , 2012, JBIC Journal of Biological Inorganic Chemistry.

[52]  Kazuya Watanabe,et al.  Microbial interspecies electron transfer via electric currents through conductive minerals , 2012, Proceedings of the National Academy of Sciences.

[53]  Leonard M Tender,et al.  On electron transport through Geobacter biofilms. , 2012, ChemSusChem.

[54]  Kelly P. Nevin,et al.  Interspecies Electron Transfer via Hydrogen and Formate Rather than Direct Electrical Connections in Cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens , 2012, Applied and Environmental Microbiology.

[55]  Jeffrey A. Gralnick,et al.  Flavin Electron Shuttles Dominate Extracellular Electron Transfer by Shewanella oneidensis , 2013, mBio.

[56]  Wen-Wei Li,et al.  Towards sustainable wastewater treatment by using microbial fuel cells-centered technologies , 2013 .

[57]  Shungui Zhou,et al.  Electron transfer capacity dependence of quinone-mediated Fe(III) reduction and current generation by Klebsiella pneumoniae L17. , 2013, Chemosphere.

[58]  Hanqing Yu,et al.  Manipulation of microbial extracellular electron transfer by changing molecular structure of phenazine-type redox mediators. , 2013, Environmental science & technology.

[59]  D. Lovley,et al.  Transcriptomic and Genetic Analysis of Direct Interspecies Electron Transfer , 2013, Applied and Environmental Microbiology.

[60]  S. Haderlein,et al.  Electron transfer between iron minerals and quinones: estimating the reduction potential of the Fe(II)-goethite surface from AQDS speciation. , 2013, Environmental science & technology.

[61]  Guohui Dong,et al.  Synthesis and Enhanced Cr(VI) Photoreduction Property of Formate Anion Containing Graphitic Carbon Nitride , 2013 .

[62]  Humic acid-enhanced electron transfer of in vivo cytochrome c as revealed by electrochemical and spectroscopic approaches. , 2014, Journal of environmental sciences.

[63]  H. Thatoi,et al.  Investigation on mechanism of Cr(VI) reduction and removal by Bacillus amyloliquefaciens, a novel chromate tolerant bacterium isolated from chromite mine soil. , 2014, Chemosphere.

[64]  Bruno M. Fonseca,et al.  Exploring the molecular mechanisms of electron shuttling across the microbe/metal space , 2014, Front. Microbiol..

[65]  Derek R Lovley,et al.  Microbial nanowires for bioenergy applications. , 2014, Current opinion in biotechnology.

[66]  Kelly P. Nevin,et al.  Promoting Interspecies Electron Transfer with Biochar , 2014, Scientific Reports.

[67]  A. Kappler,et al.  Humic substances as fully regenerable electron acceptors in recurrently anoxic environments , 2014 .

[68]  Nick Wierckx,et al.  Engineering mediator-based electroactivity in the obligate aerobic bacterium Pseudomonas putida KT2440 , 2015, Front. Microbiol..

[69]  D. Richardson,et al.  Redox Linked Flavin Sites in Extracellular Decaheme Proteins Involved in Microbe-Mineral Electron Transfer. , 2015, Scientific Reports.

[70]  Bin Cao,et al.  Enhancing Bidirectional Electron Transfer of Shewanella oneidensis by a Synthetic Flavin Pathway. , 2015, ACS synthetic biology.

[71]  S. Haderlein,et al.  Electron Transfer Between Sulfide and Humic Acid: Electrochemical Evaluation of the Reactivity of Sigma-Aldrich Humic Acid Toward Sulfide , 2016, Aquatic Geochemistry.

[72]  M. Schiffer,et al.  Bidirectional Photoinduced Electron Transfer in Ruthenium(II)-Tris-bipyridyl-Modified PpcA, a Multi-heme c-Type Cytochrome from Geobacter sulfurreducens. , 2015, The journal of physical chemistry. B.

[73]  Yaxin Tao,et al.  Environmental pH and ionic strength influence the electron-transfer capacity of dissolved organic matter , 2015, Journal of Soils and Sediments.

[74]  De-gang Fu,et al.  Carbon paper electrode modified by goethite nanowhiskers promotes bacterial extracellular electron transfer , 2015 .

[75]  C. Moon,et al.  Flavin mononucleotide mediated microbial fuel cell in the presence of Shewanella putrefaciens CN32 and iron-bearing mineral , 2015, Biotechnology and Bioprocess Engineering.

[76]  G. Reguera.  Microbes, cables, and an electrical touch. , 2015, International microbiology : the official journal of the Spanish Society for Microbiology.

[77]  Joana M. Dantas,et al.  Diving into the redox properties of Geobacter sulfurreducens cytochromes: a model for extracellular electron transfer. , 2015, Dalton transactions.

[78]  Jochen Blumberger,et al.  Multi-haem cytochromes in Shewanella oneidensis MR-1: structures, functions and opportunities , 2015, Journal of The Royal Society Interface.

[79]  Bing Li,et al.  Trace heavy metal ions promoted extracellular electron transfer and power generation by Shewanella in microbial fuel cells. , 2016, Bioresource technology.

[80]  Aidan M. McKenzie.  Ultrafast Limits of Photo-Induced Electron Transfer Rates in PPCA, a Multi-Heme C-Type Cytochrome , 2016 .

[81]  Yinguang Chen,et al.  The effects of fulvic acid on microbial denitrification: promotion of NADH generation, electron transfer, and consumption , 2016, Applied Microbiology and Biotechnology.

[82]  Fangbai Li,et al.  In Situ Spectral Kinetics of Cr(VI) Reduction by c-Type Cytochromes in A Suspension of Living Shewanella putrefaciens 200 , 2016, Scientific Reports.

[83]  Yamini Jangir,et al.  Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1 , 2016 .

[84]  O. Karlsen,et al.  Transcriptomic profiling of Methylococcus capsulatus (Bath) during growth with two different methane monooxygenases , 2015, MicrobiologyOpen.

[85]  J. Qu,et al.  3D Macroporous Nitrogen‐Enriched Graphitic Carbon Scaffold for Efficient Bioelectricity Generation in Microbial Fuel Cells , 2017 .

[86]  B. Li,et al.  Effect of the dosage of ferroferric oxide on batch anaerobic treatment of high strength synthetic wastewater , 2017 .

[87]  A. Franks,et al.  Significance of a Posttranslational Modification of the PilA Protein of Geobacter sulfurreducens for Surface Attachment, Biofilm Formation, and Growth on Insoluble Extracellular Electron Acceptors , 2017, Journal of bacteriology.

[88]  B. Li,et al.  Enhancing electron transfer by ferroferric oxide during the anaerobic treatment of synthetic wastewater with mixed organic carbon , 2017 .

[89]  Ji-ti Zhou,et al.  Microbial reduction of Fe(III)-bearing clay minerals in the presence of humic acids , 2017, Scientific Reports.

[90]  Yaobin Zhang,et al.  Potentially shifting from interspecies hydrogen transfer to direct interspecies electron transfer for syntrophic metabolism to resist acidic impact with conductive carbon cloth , 2017 .