The ins and outs of microorganism-electrode electron transfer reactions

Nature Reviews Chemistry

Volumn 1, Issue , 2017, Pages

  Kumar, Amit ^a   Hsu, Leo Huan Hsuan ^b   Kavanagh, Paul ^c   Barrière, Frédéric ^d   Lens, Piet N L ^e,f   Lapinsonnière, Laure ^d   Lienhard, John H ^a   Schröder, Uwe ^g   Jiang, Xiaocheng ^b   Leech, Dónal ^f  

^a Massachusetts Institute of Technology   (United States)

^b Tufts University   (United States)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^d UNIVERSITÉ DE RENNES 1   (France)

^e UNESCO IHE INSTITUTE FOR WATER EDUCATION   (Netherlands)

^f NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^g TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85020933729     PISSN: None     EISSN: 23973358     Source Type: Journal    
DOI: 10.1038/s41570-017-0024     Document Type: Review

References (145)

1. Rabaey, K. Bioelectrochemical Systems: From Extracellular Electron Transfer to Biotechnological Application (IWA Publishing, 2009).
2. Logan, B. E. et al. Microbial fuel cells: Methodology and technology. Environ. Sci. Technol. 40, 5181-5192 (2006).
3. Rosenbaum, M. A., Franks, A. E. Microbial catalysis in bioelectrochemical technologies: Status quo, challenges and perspectives. Appl. Microbiol. Biotechnol. 98, 509-518 (2014).
4. Wang, H., Ren, Z. J. A comprehensive review of microbial electrochemical systems as a platform technology. Biotechnol. Adv. 31, 1796-1807 (2013).
5. Bajracharya, S. et al. An overview on emerging bioelectrochemical systems (BESs): Technology for sustainable electricity, waste remediation, resource recovery, chemical production and beyond. Renew. Energy 98, 153-170 (2016).
6. Schröder, U. Anodic electron transfer mechanisms in microbial fuel cells and their energy efficiency. Phys. Chem. Chem. Phys. 9, 2619-2629 (2007).
7. Mathuriya, A. S., Yakhmi, J. V. Microbial fuel cells-applications for generation of electrical power and beyond. Crit. Rev. Microbiol. 7828, 1-17 (2014).
8. Leech, D., Kavanagh, P., Schuhmann, W. Enzymatic fuel cells: Recent progress. Electrochim. Acta 84, 223-234 (2012).
9. Habermüller, K., Mosbach, M., Schuhmann, W. Electron-transfer mechanisms in amperometric biosensors. Fresenius. J. Anal. Chem. 366, 560-568 (2000).
10. Falk, M., Blum, Z., Shleev, S. Direct electron transfer based enzymatic fuel cells. Electrochim. Acta 82, 191-202 (2012).
11. Ghindilis, A. L., Atanasov, P., Wilkins, E. Enzyme-catalyzed direct electron transfer: Fundamentals and analytical applications. Electroanalysis 9, 661-674 (1997).
12. Osman, M. H., Shah, A. A., Walsh, F. C. Recent progress and continuing challenges in bio-fuel cells. Part I: Enzymatic cells. Biosens. Bioelectron. 26, 3087-3102 (2011).
13. Schröder, U., Harnisch, F., Angenent, L. T. Microbial electrochemistry and technology: Terminology and classification. Energy Environ. Sci. 8, 513-519 (2015).
14. Willner, I., Katz, E. Integration of layered redox proteins and conductive supports for bioelectronic applications. Angew. Chem. Int. Ed. 39, 1180-1218 (2000).
15. Moehlenbrock, M. J., Minteer, S. D. Extended lifetime biofuel cells. Chem. Soc. Rev. 37, 1188-1196 (2008).
16. Kim, J., Jia, H., Wang, P. Challenges in biocatalysis for enzyme-based biofuel cells. Biotechnol. Adv. 24, 296-308 (2006).
17. Potter, M. C. Electrical effects accompanying the decomposition of organic compounds. Proc. R. Soc. Lond. B. 84, 260-276 (1911).
18. Cohen, B. The bacterial culture as an electrical half-cell. J. Bacteriol. 21, 18-19 (1931).
19. Gorby, Y. A. et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc. Natl Acad. Sci. USA 103, 11358-11363 (2006).
20. Reguera, G. et al. Extracellular electron transfer via microbial nanowires. Nature 435, 1098-1101 (2005).
21. Marsili, E. et al. Shewanella secretes flavins that mediate extracellular electron transfer. Proc. Natl Acad. Sci. USA 105, 3968-3973 (2008).
22. Newman, D. K., Kolter, R. A role for excreted quinones in extracellular electron transfer. Nature 405, 94-97 (2000).
23. Shi, L., Squier, T. C., Zachara, J. M., Fredrickson, J. K. Respiration of metal (hydr)oxides by Shewanella and Geobacter: A key role for multihaem c-type cytochromes. Mol. Microbiol. 65, 12-20 (2007).
24. Nealson, K. H., Rowe, A. R. Electromicrobiology: Realities, grand challenges, goals and predictions. Microb. Biotechnol. 9, 595-600 (2016).
25. Wei, J., Liang, P., Huang, X. Recent progress in electrodes for microbial fuel cells. Bioresour. Technol. 102, 9335-9344 (2011).
26. Torres, C. I. et al. A kinetic perspective on extracellular electron transfer by anode-respiring bacteria. FEMS Microbiol. Rev. 34, 3-17 (2010).
27. Yang, Y., Xu, M., Guo, J., Sun, G. Bacterial extracellular electron transfer in bioelectrochemical systems. Process Biochem. 47, 1707-1714 (2012).
28. Patil, S. A., Hägerhäll, C., Gorton, L. Electron transfer mechanisms between microorganisms and electrodes in bioelectrochemical systems. Bioanal. Rev. 4, 159-192 (2012).
29. Lovley, D. R., Coates, J. D., Blunt-Harris, E. L., Phillips, E. J. P., Woodward, J. C. Humic substances as electron acceptors for microbial respiration. Nature 382, 445-448 (1996).
30. Roden, E. E. et al. Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat. Geosci. 3, 417-421 (2010).
31. Ordonez, M. V., Schrott, G. D., Massazza, D. A., Busalmen, J. P. The relay network of Geobacter biofilms. Energy Environ. Sci. 9, 2677-2681 (2016).
32. Mowat, C. G., Chapman, S. K. Multi-heme cytochromes-new structures, new chemistry. Dalton Trans. 3381-3389 (2005).
33. Mehta, T., Coppi, M. V., Childers, S. E., Lovley, D. R. Outer membrane c-type cytochromes required for Fe(iii) and Mn(iv) oxide reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol. 71, 8634-8641 (2005).
34. Holmes, D. E. et al. Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. Environ. Microbiol. 8, 1805-1815 (2006).
35. Nevin, K. P. et al. Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS ONE 4, e5628 (2009).
36. Richter, H. 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. Energy Environ. Sci. 2, 506-516 (2009).
37. Coursolle, D., Baron, D. B., Bond, D. R., Gralnick, J. A. The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis. J. Bacteriol. 192, 467-474 (2010).
38. Breuer, M., Rosso, K. M., Blumberger, J., Butt, J. N. Multi-haem cytochromes in Shewanella oneidensis MR-1: Structures, functions and opportunities. J. R. Soc. Interface 12, 20141117 (2015).
39. Bond, D. R., Strycharz-Glaven, S. M., Tender, L. M., Torres, C. I. On electron transport through Geobacter biofilms. ChemSusChem 5, 1099-1105 (2012).
40. Shi, L. et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol. 14, 651-662 (2016).
41. Malvankar, N. S., Lovley, D. R. in Biofilms in Bioelectrochemical Systems: From Laboratory Practice to Data Interpretation (eds Beyenal, H., Babauta, J.) 220-222 (Wiley, 2015).
42. Xu, S., Jangir, Y., El-Naggar, M. Y. Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1. Electrochim. Acta 198, 49-55 (2016).
43. Rabaey, K., Boon, N., Siciliano, S. D., Verstraete, W., Verhaege, M. Biofuel cells select for microbial consortia that self-mediate electron transfer. Appl. Environ. Microbiol. 70, 5373-5382 (2004).
44. Shrestha, P. M., Rotaru, A. E. Plugging in or going wireless: Strategies for interspecies electron transfer. Front. Microbiol. 5, 237 (2014).
45. Malvankar, N. S. et al. Tunable metallic-like conductivity in microbial nanowire networks. Nat. Nanotechnol. 6, 573-579 (2011).
46. Pirbadian, S. et al. Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc. Natl Acad. Sci. USA 111, 12883-12888 (2014).
47. Malvankar, N. S., Rotello, V. M., Tuominen, M. T., Lovley, D. R. Reply to 'Measuring conductivity of living Geobacter sulfurreducens biofilms'. Nat. Nanotechnol. 11, 913-914 (2016).
48. Yates, M. D. et al. Measuring conductivity of living Geobacter sulfurreducens biofilms. Nat. Nanotechnol. 11, 910-913 (2016).
49. Malvankar, N. S., Lovley, D. R. Microbial nanowires: A new paradigm for biological electron transfer and bioelectronics. ChemSusChem 5, 1039-1046 (2012).
50. Malvankar, N. S., Tuominen, M. T., Lovley, D. R. Comment on "On electrical conductivity of microbial nanowires & biofilms" by S. M. Strycharz-Glaven, R. M. Snider, A. Guiseppi-Elie and L. M. Tender. Energy Environ. Sci., 2011, 4, 4366.
51. Energy Environ. Sci. 5, 6247-6249 (2012).
52. Strycharz-Glaven, S. M., Tender, L. M. Reply to the 'Comment on "On electrical conductivity of microbial nanowires & biofilms"' by N. S. Malvankar, M. T. Tuominen and D. R. Lovley. Energy Environ. Sci., 2012, 5, DOI:10.1039/c2ee02613a.
53. Energy Environ. Sci. 5, 6250-6255 (2012).
54. Strycharz-Glaven, S. M., Snider, R. M., Guiseppi-Elie, A., Tender, L. M. On the electrical conductivity of microbial nanowires and biofilms. Energy Environ. Sci. 4, 4366-4379 (2011).
55. Torres, C. I., Marcus, A. K., Parameswaran, P., Rittmann, B. E. Kinetic experiments for evaluating the Nernst-Monod model for anode-respiring bacteria (ARB) in a biofilm anode. Environ. Sci. Technol. 42, 6593-6597 (2008).
56. Yoho, R. A., Popat, S. C., Rago, L., Guisasola, A., Torres, C. I. Anode biofilms of Geoalkalibacter ferrihydriticus exhibit electrochemical signatures of multiple electron transport pathways. Langmuir 31, 12552-12559 (2015).
57. Katuri, K. P., Kavanagh, P., Rengaraj, S., Leech, D. Geobacter sulfurreducens biofilms developed under different growth conditions on glassy carbon electrodes: Insights using cyclic voltammetry. Chem. Commun. 46, 4758-4760 (2010).
58. Strycharz, S. M. et al. Application of cyclic voltammetry to investigate enhanced catalytic current generation by biofilm-modified anodes of Geobacter sulfurreducens strain DL1 vs. variant strain KN400. Energy Environ. Sci. 4, 896-913 (2011).
59. Yates, M. D. et al. Thermally activated long range electron transport in living biofilms. Phys. Chem. Chem. Phys. 17, 32564-32570 (2015).
60. Snider, R. M., Strycharz-Glaven, S. M., Tsoi, S. D., Erickson, J. S., Tender, L. M. Long-range electron transport in Geobacter sulfurreducens biofilms is redox gradient-driven. Proc. Natl Acad. Sci. USA 109, 15467-15472 (2012).
61. Schrott, G. D., Bonanni, P. S., Robuschi, L., Esteve-Nuz, A., Busalmen, J. P. Electrochemical insight into the mechanism of electron transport in biofilms of Geobacter sulfurreducens. Electrochim. Acta 56, 10791-10795 (2011).
62. El-Naggar, M. Y., Gorby, Y., Xia, W., Nealson, K. H. The molecular density of states in bacterial nanowires. Biophys. J. 95, L10-L12 (2008).
63. Pirbadian, S., El-Naggar, M. Y. Multistep hopping and extracellular charge transfer in microbial redox chains. Phys. Chem. Chem. Phys. 14, 13802-13808 (2012).
64. Yang, Y. et al. Enhancing bidirectional electron transfer of Shewanella oneidensis by a synthetic flavin pathway. ACS Synth. Biol. 4, 815-823 (2015).
65. Tao, L. et al. Improving mediated electron transport in anodic bioelectrocatalysis. Chem. Commun. 51, 12170-12173 (2015).
66. Yong, X. Y. et al. Enhancement of bioelectricity generation by manipulation of the electron shuttles synthesis pathway in microbial fuel cells. Bioresour. Technol. 152, 220-224 (2014).
67. Kirchhofer, N. D. et al. The conjugated oligoelectrolyte DSSN+ enables exceptional coulombic efficiency via direct electron transfer for anode-respiring Shewanella oneidensis MR-1-A mechanistic study. Phys. Chem. Chem. Phys. 16, 20436-20443 (2014).
68. Hou, H. et al. Conjugated oligoelectrolytes increase power generation in E. coli microbial fuel cells. Adv. Mater. 25, 1593-1597 (2013).
69. Wang, V. B. et al. Comparison of flavins and a conjugated oligoelectrolyte in stimulating extracellular electron transport from Shewanella oneidensis MR-1. Electrochem. Commun. 41, 55-58 (2014).
70. Xie, X. et al. Three-dimensional carbon nanotube textile anode for high-performance microbial fuel cells. Nano Lett. 11, 291-296 (2011).
71. Xie, X. et al. Graphene-sponges as high-performance low-cost anodes for microbial fuel cells. Energy Environ. Sci. 5, 6862-6866 (2012).
72. Ji, J. et al. A layer-by-layer self-assembled Fe2O3 nanorod-based composite multilayer film on ITO anode in microbial fuel cell. Colloids Surf. A 390, 56-61 (2011).
73. Jiang, X. et al. Nanoparticle facilitated extracellular electron transfer in microbial fuel cells. Nano Lett. 14, 6737-6742 (2014).
74. Harnisch, F., Rabaey, K. The diversity of techniques to study electrochemically active biofilms highlights the need for standardization. ChemSusChem 5, 1027-1038 (2012).
75. Millo, D. et al. In situ spectroelectrochemical investigation of electrocatalytic microbial biofilms by surface-enhanced resonance Raman spectroscopy. Angew. Chem. Int. Ed. 50, 2625-2627 (2011).
76. Liu, Y., Kim, H., Franklin, R. R., Bond, D. R. Linking spectral and electrochemical analysis to monitor c-type cytochrome redox status in living Geobacter sulfurreducens biofilms. ChemPhysChem 12, 2235-2241 (2011).
77. Lower, B. H. et al. Specific bonds between an iron oxide surface and outer membrane cytochromes MtrC and OmcA from Shewanella oneidensis MR-1. J. Bacteriol. 189, 4944-4952 (2007).
78. Li, Z., Venkataraman, A., Rosenbaum, M. A., Angenent, L. T. A laminar-flow microfluidic device for quantitative analysis of microbial electrochemical activity. ChemSusChem 5, 1119-1123 (2012).
79. Choi, S. Microscale microbial fuel cells: Advances and challenges. Biosens. Bioelectron. 69, 8-25 (2015).
80. Gross, B. J., El-Naggar, M. Y. A combined electrochemical and optical trapping platform for measuring single cell respiration rates at electrode interfaces. Rev. Sci. Instrum. 86, 064301 (2015).
81. Jiang, X. et al. Probing single-to multi-cell level charge transport in Geobacter sulfurreducens DL-1. Nat. Commun. 4, 2751 (2013).
82. Jiang, X. et al. Probing electron transfer mechanisms in Shewanella oneidensis MR-1 using a nanoelectrode platform and single-cell imaging. Proc. Natl Acad. Sci. USA 107, 16806-16810 (2010).
83. Hol, F. J. H., Dekker, C. Zooming in to see the bigger picture: Microfluidic and nanofabrication tools to study bacteria. Science 346, 1251821 (2014).
84. Weber, K. A., Achenbach, L. A., Coates, J. D. Microorganisms pumping iron: Anaerobic microbial iron oxidation and reduction. Nat. Rev. Microbiol. 4, 752-764 (2006).
85. Enning, D., Garrelfs, J. Corrosion of iron by sulfate-reducing bacteria: New views of an old problem. Appl. Environ. Microbiol. 80, 1226-1236 (2014).
86. Dinh, H. T. et al. Iron corrosion by novel anaerobic microorganisms. Nature 427, 829-832 (2004).
87. Gregory, K. B., Bond, D. R., Lovley, D. R. Graphite electrodes as electron donors for anaerobic respiration. Environ. Microbiol. 6, 596-604 (2004).
88. Ross, D. E., Flynn, J. M., Baron, D. B., Gralnick, J. A., Bond, D. R. Towards electrosynthesis in Shewanella: Energetics of reversing the Mtr pathway for reductive metabolism. PLoS ONE 6, e16649 (2011).
89. Strycharz, S. M. et al. Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens. Bioelectrochemistry 80, 142-150 (2011).
90. Tremblay, P. L., Zhang, T. Electrifying microbes for the production of chemicals. Front. Microbiol. 6, 201 (2015).
91. Strycharz, S. M. et al. Graphite electrode as a sole electron donor for reductive dechlorination of tetrachlorethene by Geobacter lovleyi. Appl. Environ. Microbiol. 74, 5943-5947 (2008).
92. Hsu, L., Masuda, S. A., Nealson, K. H., Pirbazari, M. Evaluation of microbial fuel cell Shewanella biocathodes for treatment of chromate contamination. RSC Adv. 2, 5844-5855 (2012).
93. Gregory, K. B., Lovley, D. R. Remediation and recovery of uranium from contaminated subsurface environments with electrodes. Environ. Sci. Technol. 39, 8943-8947 (2005).
94. Williams, K. H., Bargar, J. R., Lloyd, J. R., Lovley, D. R. Bioremediation of uranium-contaminated groundwater: A systems approach to subsurface biogeochemistry. Curr. Opin. Biotechnol. 24, 489-497 (2013).
95. Rabaey, K., Rozendal, R. A. Microbial electrosynthesis-revisiting the electrical route for microbial production. Nat. Rev. Microbiol. 8, 706-716 (2010).
96. Nevin, K. P., Woodard, T. L., Franks, A. E., Summers, Z. M., Lovley, D. R. Microbial electrosynthesis: Feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. mBio 1, e00103-10 (2010).
97. Nevin, K. P. et al. Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl. Environ. Microbiol. 77, 2882-2886 (2011).
98. Choi, O., Kim, T., Woo, H. M., Um, Y. Electricity-driven metabolic shift through direct electron uptake by electroactive heterotroph Clostridium pasteurianum. Sci. Rep. 4, 6961 (2014).
99. Cheng, S., Xing, D., Call, D. F., Logan, B. E. Direct biological conversion of electrical current into methane by electromethanogenesis. Environ. Sci. Technol. 43, 3953-3958 (2009).
100. Deutzmann, J. S., Sahin, M., Spormann, A. M. Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis. mBio 6, e00496-15 (2015).
101. Bose, A., Gardel, E. J., Vidoudez, C., Parra, E. A., Girguis, P. R. Electron uptake by iron-oxidizing phototrophic bacteria. Nat. Commun. 5, 3391 (2014).
102. Deng, X., Nakamura, R., Hashimoto, K., Okamoto, A. Electron extraction from an extracellular electrode by Desulfovibrio ferrophilus strain IS5 without using hydrogen as an electron carrier. Electrochemistry 83, 529-531 (2015).
103. Claassens, N. J., Sousa, D. Z., Martins dos Santos, V. A. P., de Vos, W. M., van der Oost, J. Harnessing the power of microbial autotrophy. Nat. Rev. Microbiol. 14, 692-706 (2016).
104. Kavanagh, P., Leech, D. Mediated electron transfer in glucose oxidising enzyme electrodes for application to biofuel cells: Recent progress and perspectives. Phys. Chem. Chem. Phys. 15, 4859-4869 (2013).
105. Gallaway, J. W., Calabrese Barton, S. A. Kinetics of redox polymer-mediated enzyme electrodes. J. Am. Chem. Soc. 130, 8527-8536 (2008).
106. Liu, J. L., Lowy, D. A., Baumann, R. G., Tender, L. M. Influence of anode pretreatment on its microbial colonization. J. Appl. Microbiol. 102, 177-183 (2007).
107. Saito, T. et al. Effect of nitrogen addition on the performance of microbial fuel cell anodes. Bioresour. Technol. 102, 395-398 (2011).
108. Guo, K. et al. Effects of surface charge and hydrophobicity on anodic biofilm formation, community composition, and current generation in bioelectrochemical systems. Environ. Sci. Technol. 47, 7563-7570 (2013).
109. Kumar, A., Conghaile, P. O., Katuri, K., Lens, P., Leech, D. Arylamine functionalization of carbon anodes for improved microbial electrocatalysis. RSC Adv. 3, 18759-18761 (2013).
110. Guo, K. et al. Flame oxidation of stainless steel felt enhances anodic biofilm formation and current output in bioelectrochemical systems. Environ. Sci. Technol. 48, 7151-7156 (2014).
111. Liu, X. W., Li, W.-W., Yu, H. Q. Cathodic catalysts in bioelectrochemical systems for energy recovery from wastewater. Chem. Soc. Rev. 43, 7718-7745 (2014).
112. Jourdin, L. et al. A novel carbon nanotube modified scaffold as an efficient biocathode material for improved microbial electrosynthesis. J. Mater. Chem. A 2, 13093-13102 (2014).
113. Marsili, E., Sun, J., Bond, D. R. Voltammetry and growth physiology of Geobacter sulfurreducens biofilms as a function of growth stage and imposed electrode potential. Electroanalysis 22, 865-874 (2010).
114. Dumas, C., Basseguy, R., Bergel, A. Electrochemical activity of Geobacter sulfurreducens biofilms on stainless steel anodes. Electrochim. Acta 53, 5235-5241 (2008).
115. Erable, B. et al. Marine aerobic biofilm as biocathode catalyst. Bioelectrochemistry 78, 51-56 (2010).
116. Finkelstein, D. A., Tender, L. M., Zeikus, J. G. Effect of electrode potential on electrode-reducing microbiota. Environ. Sci. Technol. 40, 6990-6995 (2006).
117. Picot, M., Lapinsonnière, L., Rothballer, M., Barrière, F. Graphite anode surface modification with controlled reduction of specific aryl diazonium salts for improved microbial fuel cells power output. Biosens. Bioelectron. 28, 181-188 (2011).
118. Smith, R. A. J., Porteous, C. M., Gane, A. M., Murphy, M. P. Delivery of bioactive molecules to mitochondria in vivo. Proc. Natl Acad. Sci. USA 100, 5407-5412 (2003).
119. Lapinsonnière, L., Picot, M., Poriel, C., Barrière, F. Phenylboronic acid modified anodes promote faster biofilm adhesion and increase microbial fuel cell performances. Electroanalysis 25, 601-605 (2013).
120. Ding, C., Lv, M., Zhu, Y., Jiang, L., Liu, H. Wettability-regulated extracellular electron transfer from the living organism of Shewanella loihica PV-4. Angew. Chem. Int. Ed. 54, 1446-1451 (2015).
121. Parameswaran, P., Torres, C. I., Lee, H. S., Krajmalnik-Brown, R., Rittmann, B. E. Syntrophic interactions among anode respiring bacteria (ARB) and non-ARB in a biofilm anode: Electron balances. Biotechnol. Bioeng. 103, 513-523 (2009).
122. Cracknell, J. A., Vincent, K. A., Armstrong, F. A. Enzymes as working or inspirational electrocatalysts for fuel cells and electrolysis. Chem. Rev. 108, 2439-2461 (2008).
123. El Kasmi, A., Wallace, J. M., Bowden, E. F., Binet, S. M., Linderman, R. J. Controlling interfacial electron-transfer kinetics of cytochrome c with mixed self-assembled monolayers. J. Am. Chem. Soc. 120, 225-226 (1998).
124. Wang, G. X., Bao, W. J., Wang, M., Xia, X. H. Heme plane orientation dependent direct electron transfer of cytochrome c at SAMs/Au electrodes with different wettability. Chem. Commun. 48, 10859-10861 (2012).
125. Song, S., Clark, R. A., Bowden, E. F., Tarlov, M. J. Characterization of cytochrome c/alkanethiolate structures prepared by self-assembly on gold. J. Phys. Chem. 97, 6564-6572 (1993).
126. Hasan, K., Patil, S., Leech, D., Hägerhäll, C., Gorton, L. Electrochemical communication between microbial cells and electrodes via osmium redox systems. Biochem. Soc. Trans. 40, 1330-1335 (2012).
127. Ghach, W., Etienne, M., Urbanova, V., Jorand, F. P. A., Walcarius, A. Sol-gel based 'artificial' biofilm from Pseudomonas fluorescens using bovine heart cytochrome c as electron mediator. Electrochem. Commun. 38, 71-74 (2014).
128. Heller, A. Electrical wiring of redox enzymes. Acc. Chem. Res. 23, 128-134 (1990).
129. Hamidi, H. et al. Photocurrent generation from thylakoid membranes on osmium-redox-polymer-modified electrodes. ChemSusChem 8, 990-993 (2015).
130. Hasan, K. et al. Photo-electrochemical communication between cyanobacteria (Leptolyngbia sp.) and osmium redox polymer modified electrodes. Phys. Chem. Chem. Phys. 16, 24676-24680 (2014).
131. Nie, H. et al. Improved cathode for high efficient microbial-catalyzed reduction in microbial electrosynthesis cells. Phys. Chem. Chem. Phys. 15, 14290-14294 (2013).
132. Zhang, T. et al. Improved cathode materials for microbial electrosynthesis. Energy Environ. Sci. 6, 217-224 (2013).
133. Popat, S. C., Ki, D., Rittmann, B. E., Torres, C. I. Importance of OH transport from cathodes in microbial fuel cells. ChemSusChem 5, 1071-1079 (2012).
134. Lebedev, N., Strycharz-Glaven, S. M., Tender, L. M. High resolution AFM and single-cell resonance Raman spectroscopy of Geobacter sulfurreducens biofilms early in growth. Front. Energy Res. 2, 34 (2014).
135. Kumar, A. et al. Catalytic response of microbial biofilms grown under fixed anode potentials depends on electrochemical cell configuration. Chem. Eng. J. 230, 532-536 (2013).
136. Jana, P. S., Katuri, K., Kavanagh, P., Kumar, A., Leech, D. Charge transport in films of Geobacter sulfurreducens on graphite electrodes as a function of film thickness. Phys. Chem. Chem. Phys. 16, 9039-9046 (2014).
137. Kumar, A., Katuri, K., Lens, P., Leech, D. Does bioelectrochemical cell configuration and anode potential affect biofilm response Biochem. Soc. Trans. 40, 1308-1314 (2012).
138. Tender, L. M. et al. The first demonstration of a microbial fuel cell as a viable power supply: Powering a meteorological buoy. J. Power Sources 179, 571-575 (2008).
139. Chaudhuri, S. K., Lovley, D. R. Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells. Nat. Biotechnol. 21, 1229-1232 (2003).
140. Kim, H. J. et al. A mediator-less microbial fuel cell using a metal reducing bacterium, Shewanella putrefaciens. Enzyme Microb. Technol. 30, 145-152 (2002).
141. Lovley, D. R., Phillips, E. J. P. Novel mode of microbial energy metabolism: Organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54, 1472-1480 (1988).
142. Myers, C. R., Nealson, K. H. Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240, 1319-1321 (1988).
143. Yates, M. D. et al. Toward understanding long-distance extracellular electron transport in an electroautotrophic microbial community. Energy Environ. Sci. 9, 3544-3588 (2016).
144. Ueki, T., Nevin, K. P., Woodard, T. L., Lovley, D. R. Converting carbon dioxide to butyrate with an engineered strain of Clostridium ljungdahlii. mBio 5, e01636-14 (2014).
145. Kane, A. L., Bond, D. R., Gralnick, J. A. Electrochemical analysis of Shewanella oneidensis engineered to bind gold electrodes. ACS Synth. Biol. 2, 93-101 (2013).