Microbial electron transport and energy conservation - The foundation for optimizing bioelectrochemical systems

Frontiers in Microbiology

Volumn 6, Issue JUN, 2015, Pages

  Kracke, Frauke ^a   Vassilev, Igor ^a   Krömer, Jens O ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Acetogenic bacteria; ATP yield; Bio electrochemistry; Bioelectrochemical system; Microbial electron transport; Microbial electrosynthesis; Microbial fuel cell; Redox potential

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME; FERREDOXIN; FERRIC ION; FLAVINE ADENINE NUCLEOTIDE; HYDROQUINONE; MANGANESE OXIDE; MENAQUINONE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PHENAZINE; QUINONE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ACETOBACTERIUM WOODII; BACTERIUM; BIOFILM; CARBON METABOLISM; CLOSTRIDIUM LJUNGDAHLII; CORYNEBACTERIUM GLUTAMICUM; ELECTROCHEMISTRY; ELECTRODE; ELECTRON TRANSPORT; ENERGY CONSERVATION; ENERGY METABOLISM; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; GEOBACTER SULFURREDUCENS; MICROBIAL ELECTRON TRANSPORT; MICROBIAL ELECTROSYNTHESIS; MICROBIAL FUEL CELL; MICROBIAL METABOLISM; MOORELLA THERMOACETICA; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; RESPIRATORY CHAIN; REVIEW; SHEWANELLA ONEIDENSIS; SIGNAL TRANSDUCTION;

EID: 84936993627     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00575     Document Type: Review

References (147)

1. Anraku, Y. (1988). Bacterial electron transport chains. Annu. Rev. Biochem. 57, 101-132. doi: 10.1146/annurev.bi.57.070188.000533
2. Atkinson, S. J., Mowat, C. G., Reid, G. A., and Chapman, S. K. (2007). An octaheme c-type cytochrome from Shewanella oneidensis can reduce nitrite and hydroxylamine. FEBS Lett. 581, 3805-3808. doi: 10.1016/j.febslet.2007.07.005
3. Baltch, A. L., and Smith, R. P. (eds). (1994). Pseudomonas aeruginosa: Infections and Treatment. New York, NY: Marcel Dekker, Inc.
4. Banerjee, A., Leang, C., Ueki, T., Nevin, K. P., and Lovley, D. R. (2014). Lactose-inducible system for metabolic engineering of Clostridium ljungdahlii. Appl. Environ. Microbiol. 80, 2410-2416. doi: 10.1128/AEM.03666-13
5. Berlyn, M. K. (1998). Linkage map of Escherichia coli K-10: the traditional map. Microbiol. Mol. Biol. Rev. 62, 814-984.
6. Bertini, I., Cavallaro, G., and Rosato, A. (2006). Cytochrome c: occurrence and functions. Chem. Rev. 106, 90-115. doi: 10.1021/cr050241v
7. Biegel, E., Schmidt, S., González, J., and Müller, V. (2011). Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes. Cell. Mol. Life Sci. 68, 613-634. doi: 10.1007/s00018-010-0555-8
8. Bond, D. R., and Lovley, D. R. (2003). Electricity production by Geobacter sulfurreducens attached to electrodes. Appl. Environ. Microbiol. 69, 1548-1555. doi: 10.1128/aem.69.3.1548-1555.2003
9. Boon, N., De Maeyer, K., Höfte, M., Rabaey, K., and Verstraete, W. (2008). Use of Pseudomonas species producing phenazine-based metabolites in the anodes of microbial fuel cells to improve electricity generation. Appl. Microbiol. Biotechnol. 80, 985-993. doi: 10.1007/s00253-008-1619-7
10. Bott, M., and Niebisch, A. (2003). The respiratory chain of Corynebacterium glutamicum. J. Biotechnol. 104, 129-153. doi: 10.1016/S0168-1656(03)00144-5
11. Breuer, M., Rosso, K. M., Blumberger, J., and Butt, J. N. (2015). Multi-haem cytochromes in Shewanella oneidensis MR-1: structures, functions and opportunities. J. R. Soc. Interface 12, 20141117. doi: 10.1098/rsif.2014.1117
12. Buckel, W., and Thauer, R. K. (2013). Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation. Biochim. Biophys. Acta 1827, 94-113. doi: 10.1016/j.bbabio.2012.07.002
13. Carlson, H. K., Iavarone, A. T., Gorur, A., Yeo, B. S., Tran, R., Melnyk, R. A., et al. (2012). Surface multiheme c-type cytochromes from Thermincola potens and implications for respiratory metal reduction by Gram-positive bacteria. Proc. Natl. Acad. Sci. U.S.A. 109, 1702-1707. doi: 10.1073/pnas.1112905109
14. Choi, O., Um, Y., and Sang, B.-I. (2012). Butyrate production enhancement by Clostridium tyrobutyricum using electron mediators and a cathodic electron donor. Biotechnol. Bioeng. 109, 2494-2502. doi: 10.1002/bit.24520
15. Coursolle, D., and Gralnick, J. A. (2010). Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol. Microbiol. 77, 995-1008. doi: 10.1111/j.1365-2958.2010.07266.x
16. Das, A., and Ljungdahl, L. G. (2003). "Electron-transport system in acetogens," in Biochemistry and Physiology of Anaerobic Bacteria, eds L. G. Ljungdahl, M. W. Adams, L. Barton, J. G. Ferry, and M. K. Johnson (New York, NY: Springer-Verlag), 191-204. doi: 10.1007/0-387-22731-8_14
17. Deller, S., Macheroux, P., and Sollner, S. (2008). Flavin-dependent quinone reductases. Cell. Mol. Life Sci. 65, 141-160. doi: 10.1007/s00018-007-7300-y
18. Deutzmann, J. S., Sahin, M., and Spormann, A. M. (2015). Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis. MBio 6:e00496-15. doi: 10.1128/mBio.00496-15
19. Diekert, G., and Wohlfarth, G. (1994). Metabolism of homoacetogens. Antonie Van Leeuwenhoek 66, 209-221. doi: 10.1007/BF00871640
20. Dolin, M. (2012). Survey of microbial electron transport mechanisms. Bacteria 2:319.
21. Dos Santos, J.-P., Iobbi-Nivol, C., Couillault, C., Giordano, G., and Méjean, V. (1998). Molecular analysis of the trimethylamine N-oxide (TMAO) reductase respiratory system from a Shewanella species. J. Mol. Biol. 284, 421-433. doi: 10.1006/jmbi.1998.2155
22. Drake, H. L., Gößner, A. S., and Daniel, S. L. (2008). Old acetogens, new light. Ann. N. Y. Acad. Sci. 1125, 100-128. doi: 10.1196/annals.1419.016
23. Dumas, C., Basseguy, R., and Bergel, A. (2008). Microbial electrocatalysis with Geobacter sulfurreducens biofilm on stainless steel cathodes. Electrochim. Acta 53, 2494-2500. doi: 10.1016/j.electacta.2007.10.018
24. Emde, R., and Schink, B. (1990). Enhanced propionate formation by Propionibacterium freudenreichii subsp. freudenreichii in a three-electrode amperometric culture system. Appl. Environ. Microbiol. 56, 2771-2776.
25. Fast, A. G., and Papoutsakis, E. T. (2012). Stoichiometric and energetic analyses of non-photosynthetic CO2-fixation pathways to support synthetic biology strategies for production of fuels and chemicals. Curr. Opin. Chem. Eng. 1, 380-395. doi: 10.1016/j.coche.2012.07.005
26. Firer-Sherwood, M., Pulcu, G. S., and Elliott, S. J. (2008). Electrochemical interrogations of the Mtr cytochromes from Shewanella: opening a potential window. J. Biol. Inorg. Chem. 13, 849-854. doi: 10.1007/s00775-008-0398-z
27. Fonseca, B. M., Paquete, C. M., Neto, S. E., Pacheco, I., Soares, C. M., and Louro, R. O. (2013). Mind the gap: cytochrome interactions reveal electron pathways across the periplasm of Shewanella oneidensis MR-1. Biochem. J. 449, 101-108. doi: 10.1042/BJ20121467
28. Franks, A. (2012). What's current with electric microbes. J. Bacteriol. Parasitol. 3:e116. doi: 10.4172/2155-9597.1000e116
29. Franks, A. E., and Nevin, K. P. (2010). Microbial fuel cells, a current review. Energies 3, 899-919. doi: 10.3390/en3050899
30. Gao, H., Yang, Z. K., Barua, S., Reed, S. B., Romine, M. F., Nealson, K. H., et al. (2009). Reduction of nitrate in Shewanella oneidensis depends on atypical NAP and NRF systems with NapB as a preferred electron transport protein from CymA to NapA. ISME J. 3, 966-976. doi: 10.1038/ismej.2009.40
31. Gescher, J. S., Cordova, C. D., and Spormann, A. M. (2008). Dissimilatory iron reduction in Escherichia coli: identification of CymA of Shewanella oneidensis and NapC of E. coli as ferric reductases. Mol. Microbiol. 68, 706-719. doi: 10.1111/j.1365-2958.2008.06183.x
32. Gralnick, J. A., Vali, H., Lies, D. P., and Newman, D. K. (2006). Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc. Natl. Acad. Sci. U.S.A. 103, 4669-4674. doi: 10.1073/pnas.0505959103
33. Gregory, K. B., Bond, D. R., and Lovley, D. R. (2004). Graphite electrodes as electron donors for anaerobic respiration. Environ. Microbiol. 6, 596-604. doi: 10.1111/j.1462-2920.2004.00593.x
34. Haddock, B. A., and Schairer, H. U. (1973). Electron-transport chains of Escherichia coli. Eur. J. Biochem. 35, 34-45. doi: 10.1111/j.1432-1033.1973.tb02806.x
35. Hannemann, F., Bichet, A., Ewen, K. M., and Bernhardt, R. (2007). Cytochrome P450 systems-biological variations of electron transport chains. Biochim. Biophys. Acta 1770, 330-344. doi: 10.1016/j.bbagen.2006.07.017
36. Harnisch, F., Rosa, L. F., Kracke, F., Virdis, B., and Krömer, J. O. (2014). Electrifying white biotechnology: engineering and economic potential of electricity-driven bio-production. ChemSusChem 8, 758-766. doi: 10.1002/cssc.201402736
37. Hartshorne, R. S., Reardon, C. L., Ross, D., Nuester, J., Clarke, T. A., Gates, A. J., et al. (2009). Characterization of an electron conduit between bacteria and the extracellular environment. Proc. Natl. Acad. Sci. U.S.A. 106, 22169-22174. doi: 10.1073/pnas.0900086106
38. Hassett, D. J., Cuppoletti, J., Trapnell, B., Lymar, S. V., Rowe, J. J., Yoon, S. S., et al. (2002). Anaerobic metabolism and quorum sensing by Pseudomonas aeruginosa biofilms in chronically infected cystic fibrosis airways: rethinking antibiotic treatment strategies and drug targets. Adv. Drug Del. Rev. 54, 1425-1443. doi: 10.1016/S0169-409X(02)00152-7
39. Heidelberg, J. F., Paulsen, I. T., Nelson, K. E., Gaidos, E. J., Nelson, W. C., Read, T. D., et al. (2002). Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat. Biotechnol. 20, 1118-1123. doi: 10.1038/nbt749
40. Hernandez, M. E., Kappler, A., and Newman, D. K. (2004). Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl. Environ. Microbiol. 70, 921-928. doi: 10.1128/AEM.70.2.921-928.2004
41. Hernandez, M., and Newman, D. (2001). Extracellular electron transfer. Cell. Mol. Life Sci. 58, 1562-1571. doi: 10.1007/PL00000796
42. Herrmann, G., Jayamani, E., Mai, G., and Buckel, W. (2008). Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J. Bacteriol. 190, 784-791. doi: 10.1128/JB.01422-07
43. Hess, V., Schuchmann, K., and Müller, V. (2013). The ferredoxin: NAD+ oxidoreductase (Rnf) from the acetogen Acetobacterium woodii requires Na+ and is reversibly coupled to the membrane potential. J. Biol. Chem. 288, 31496-31502. doi: 10.1074/jbc.M113.510255
44. Holmes, D. E., Chaudhuri, S. K., Nevin, K. P., Mehta, T., Methé, B. A., Liu, A., et al. (2006). Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. Environ. Microbiol. 8, 1805-1815. doi: 10.1111/j.1462-2920.2006.01065.x
45. Huang, H., Wang, S., Moll, J., and Thauer, R. K. (2012). Electron bifurcation involved in the energy metabolism of the acetogenic bacterium Moorella thermoacetica growing on glucose or H2 plus CO2. J. Bacteriol. 194, 3689-3699. doi: 10.1128/JB.00385-12
46. Ingledew, W. J. (1983). The electron transport chain of Escherichia coli grown anaerobically with fumarate as terminal electron acceptor: an electron paramagnetic resonance study. J. Gen. Microbiol. 129, 1651-1659. doi: 10.1099/00221287-129-6-1651
47. Inoue, K., Qian, X., Morgado, L., Kim, B.-C., Mester, T., Izallalen, M., et al. (2010). Purification and characterization of OmcZ, an outer-surface, octaheme c-type cytochrome essential for optimal current production by Geobacter sulfurreducens. Appl. Environ. Microbiol. 76, 3999-4007. doi: 10.1128/AEM.00027-10
48. Janicek, A., Fan, Y., and Liu, H. (2014). Design of microbial fuel cells for practical application: a review and analysis of scale-up studies. Biofuels 5, 79-92. doi: 10.4155/bfs.13.69
49. Jensen, H. M., Albers, A. E., Malley, K. R., Londer, Y. Y., Cohen, B. E., Helms, B. A., et al. (2010). Engineering of a synthetic electron conduit in living cells. Proc. Natl. Acad. Sci. U.S.A. 107, 19213-19218. doi: 10.1073/pnas.1009645107
50. Jo, J., Price-Whelan, A., and Dietrich, L. E. (2014). An aerobic exercise: defining the roles of Pseudomonas aeruginosa terminal oxidases. J. Bacteriol. 196, 4203-4205. doi: 10.1128/JB.02336-14
51. Kim, B.-C., Postier, B. L., Didonato, R. J., Chaudhuri, S. K., Nevin, K. P., and Lovley, D. R. (2008). Insights into genes involved in electricity generation in Geobacter sulfurreducens via whole genome microarray analysis of the OmcF-deficient mutant. Bioelectrochemistry 73, 70-75. doi: 10.1016/j.bioelechem.2008.04.023
52. Kim, B.-C., Qian, X., Leang, C., Coppi, M. V., and Lovley, D. R. (2006). Two putative c-type multiheme cytochromes required for the expression of OmcB, an outer membrane protein essential for optimal Fe (III) reduction in Geobacter sulfurreducens. J. Bacteriol. 188, 3138-3142. doi: 10.1128/JB.188.8.3138-3142.2006
53. Kim, T. S., and Kim, B. H. (1988). Electron flow shift in Clostridium acetobutylicum fermentation by electrochemically introduced reducing equivalent. Biotechnol. Lett. 10, 123-128. doi: 10.1007/BF01024638
54. Köpke, M., Held, C., Hujer, S., Liesegang, H., Wiezer, A., Wollherr, A., et al. (2010). Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc. Natl. Acad. Sci. U.S.A. 107, 13087-13092. doi: 10.1073/pnas.1004716107
55. Kracke, F., and Krömer, J. O. (2014). Identifying target processes for microbial electrosynthesis by elementary mode analysis. BMC Bioinformatics 15:6590. doi: 10.1186/s12859-014-0410-2
56. Leang, C., and Lovley, D. R. (2005). Regulation of two highly similar genes, omcB and omcC, in a 10 kb chromosomal duplication in Geobacter sulfurreducens. Microbiology 151, 1761-1767. doi: 10.1099/mic.0.27870-0
57. Lee, J., Jang, Y.-S., Choi, S. J., Im, J. A., Song, H., Cho, J. H., et al. (2012). Metabolic engineering of Clostridium acetobutylicum ATCC 824 for isopropanol-butanol-ethanol fermentation. Appl. Environ. Microbiol. 78, 1416-1423. doi: 10.1128/AEM.06382-11
58. Levar, C., Rollefson, J., and Bond, D. (2012). "Energetic and molecular constraints on the mechanism of environmental Fe (III) reduction by Geobacter," in Microbial Metal Respiration, eds J. Gescher and A. Kappler (Berlin: Springer), 29-48.
59. Lloyd, J., Leang, C., Hodges, M. A., Coppi, M., Cuifo, S., Methe, B., et al. (2003). Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochem. J. 369, 153-161. doi: 10.1042/BJ20020597
60. Logan, B. E. (2009). Exoelectrogenic bacteria that power microbial fuel cells. Nat. Rev. Microbiol. 7, 375-381. doi: 10.1038/nrmicro2113
61. Logan, B. E., and Rabaey, K. (2012). Conversion of wastes into bioelectricity and chemicals by using microbial electrochemical technologies. Science 337, 686-690. doi: 10.1126/science.1217412
62. Lovley, D. R. (2012). Electromicrobiology. Annu. Rev. Microbiol. 66, 391-409. doi: 10.1146/annurev-micro-092611-150104
63. Lovley, D. R., Holmes, D. E., and Nevin, K. P. (2004). Dissimilatory fe (iii) and mn (iv) reduction. Adv. Microb. Physiol. 49, 219-286. doi: 10.1016/s0065-2911(04)49005-5
64. Lovley, D. R., and Nevin, K. P. (2013). Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity. Curr. Opin. Biotechnol. 24, 385-390. doi: 10.1016/j.copbio.2013.02.012
65. Lower, B. H., Hochella, M. F., and Lower, S. K. (2005). Putative mineral-specific proteins synthesized by a metal reducing bacterium. Am. J. Sci. 305, 687-710. doi: 10.2475/ajs.305.6-8.687
66. Lütke-Eversloh, T., and Bahl, H. (2011). Metabolic engineering of Clostridium acetobutylicum: recent advances to improve butanol production. Curr. Opin. Biotechnol. 22, 634-647. doi: 10.1016/j.copbio.2011.01.011
67. Maier, T. M., Myers, J. M., and Myers, C. R. (2003). Identification of the gene encoding the sole physiological fumarate reductase in Shewanella oneidensis MR-1. J. Basic Microbiol. 43, 312-327. doi: 10.1002/jobm.200390034
68. Malvankar, N. S., Tuominen, M. T., and Lovley, D. R. (2012). Comment on "On Electrical Conductivity of Microbial Nanowires and Biofilms" by S. M. Strycharz-Glaven, R. M. Snider, A. Guiseppi-Elie, and L. M. Tender, Energy Environ. Sci. 2011, 4, 4366. Energy Environ. Sci. 5, 6247-6249. doi: 10.1039/c2ee02613a
69. Malvankar, N. S., Vargas, M., Nevin, K. P., Franks, A. E., Leang, C., Kim, B.-C., et al. (2011). Tunable metallic-like conductivity in microbial nanowire networks. Nat. Nanotechnol. 6, 573-579. doi: 10.1038/nnano.2011.119
70. Malvankar, N. S., Vargas, M., Nevin, K., Tremblay, P.-L., Evans-Lutterodt, K., Nykypanchuk, D., et al. (2015). Structural basis for metallic-like conductivity in microbial nanowires. MBio 6:e00084-15. doi: 10.1128/mBio.00084-15
71. Marshall, C. W., and May, H. D. (2009). Electrochemical evidence of direct electrode reduction by a thermophilic gram-positive bacterium, Thermincola ferriacetica. Energy Environ. Sci. 2, 699-705. doi: 10.1039/b823237g
72. Marshall, C. W., Ross, D. E., Fichot, E. B., Norman, R. S., and May, H. D. (2012). Electrosynthesis of commodity chemicals by an autotrophic microbial community. Appl. Environ. Microbiol. 78, 8412-8420. doi: 10.1128/AEM.02401-12
73. Marsili, E., Baron, D. B., Shikhare, I. D., Coursolle, D., Gralnick, J. A., and Bond, D. R. (2008a). Shewanella secretes flavins that mediate extracellular electron transfer. Proc. Natl. Acad. Sci. U.S.A. 105, 3968-3973. doi: 10.1073/pnas.0710525105
74. Marsili, E., Rollefson, J. B., Baron, D. B., Hozalski, R. M., and Bond, D. R. (2008b). Microbial biofilm voltammetry: direct electrochemical characterization of catalytic electrode-attached biofilms. Appl. Environ. Microbiol. 74, 7329-7337. doi: 10.1128/AEM.00177-08
75. Mehta, T., Coppi, M. V., Childers, S. E., and Lovley, D. R. (2005). Outer membrane c-type cytochromes required for Fe (III) and Mn (IV) oxide reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol. 71, 8634-8641. doi: 10.1128/AEM.71.12.8634-8641.2005
76. Methe, B., Nelson, K. E., Eisen, J., Paulsen, I., Nelson, W., Heidelberg, J., et al. (2003). Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302, 1967-1969. doi: 10.1126/science.1088727
77. Møller, J. V., Juul, B., and Le Maire, M. (1996). Structural organization, ion transport, and energy transduction of P-type ATPases. Biochim. Biophys. Acta Rev. Biomembr. 1286, 1-51. doi: 10.1016/0304-4157(95)00017-8
78. Morgado, L., Bruix, M., Pessanha, M., Londer, Y. Y., and Salgueiro, C. A. (2010). Thermodynamic characterization of a triheme cytochrome family from Geobacter sulfurreducens reveals mechanistic and functional diversity. Biophys. J. 99, 293-301. doi: 10.1016/j.bpj.2010.04.017
79. Müller, V. (2003). Energy conservation in acetogenic bacteria. Appl. Environ. Microbiol. 69, 6345-6353. doi: 10.1128/AEM.69.11.6345-6353.2003
80. Müller, V., and Frerichs, J. (2013). "Acetogenic bacteria," in Encyclopedia of Life Sciences (Chichester: John Wiley & Sons), 1-9. doi: 10.1002/9780470015902.a0020086.pub2
81. Müller, V., Imkamp, F., Biegel, E., Schmidt, S., and Dilling, S. (2008). Discovery of a Ferredoxin: NAD+-Oxidoreductase (Rnf) in Acetobacterium woodii. Ann. N. Y. Acad. Sci. 1125, 137-146. doi: 10.1196/annals.1419.011
82. Myers, J. M., and Myers, C. R. (2000). Role of the tetraheme cytochrome CymA in anaerobic electron transport in cells of Shewanella putrefaciens MR-1 with normal levels of menaquinone. J. Bacteriol. 182, 67-75. doi: 10.1128/JB.182.1.67-75.2000
83. Nevin, K. P., Hensley, S. A., Franks, A. E., Summers, Z. M., Ou, J., Woodard, T. L., et al. (2011). Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl. Environ. Microbiol. 77, 2882-2886. doi: 10.1128/em.02642-10
84. Nevin, K. P., Kim, B.-C., Glaven, R. H., Johnson, J. P., Woodard, T. L., Methé, B. A., et al. (2009). Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS ONE 4:e5628. doi: 10.1371/journal.pone.0005628
85. Nevin, K. P., Woodard, T. L., Franks, A. E., Summers, Z. M., and Lovley, D. R. (2010). Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. MBio 1, e00103-e00110. doi: 10.1128/mBio.00103-10
86. Nishimura, T., Vertès, A. A., Shinoda, Y., Inui, M., and Yukawa, H. (2007). Anaerobic growth of Corynebacterium glutamicum using nitrate as a terminal electron acceptor. Appl. Microbiol. Biotechnol. 75, 889-897. doi: 10.1007/s00253-007-0879-y
87. Noguchi, Y., Nakai, Y., Shimba, N., Toyosaki, H., Kawahara, Y., Sugimoto, S., et al. (2004). The energetic conversion competence of Escherichia coli during aerobic respiration studied by 31P NMR using a circulating fermentation system. J. Biochem. 136, 509-515. doi: 10.1093/jb/mvh147
88. Okamoto, A., Hashimoto, K., Nealson, K. H., and Nakamura, R. (2013). Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones. Proc. Natl. Acad. Sci. U.S.A. 110, 7856-7861. doi: 10.1073/pnas.1220823110
89. Okamoto, A., Saito, K., Inoue, K., Nealson, K. H., Hashimoto, K., and Nakamura, R. (2014). Uptake of self-secreted flavins as bound cofactors for extracellular electron transfer in Geobacter species. Energy Environ. Sci. 7, 1357-1361. doi: 10.1039/c3ee43674h
90. Parameswaran, P., Bry, T., Popat, S. C., Lusk, B. G., Rittmann, B. E., and Torres, C. I. (2013). Kinetic, electrochemical, and microscopic characterization of the thermophilic, anode-respiring bacterium Thermincola ferriacetica. Environ. Sci. Technol. 47, 4934-4940. doi: 10.1021/es400321c
91. Patil, S. A., Haegerhaell, C., and Gortin, L. (2012). Electron transfer mechanisms between microorganisms and electrodes in bioelectrochemical systems. Bioanal. Rev. 4, 159-192. doi: 10.1007/s12566-012-0033-x
92. Pierce, E., Xie, G., Barabote, R. D., Saunders, E., Han, C. S., Detter, J. C., et al. (2008). The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum). Environ. Microbiol. 10, 2550-2573. doi: 10.1111/j.1462-2920.2008.01679.x
93. Pirbadian, S., Barchinger, S. E., Leung, K. M., Byun, H. S., Jangir, Y., Bouhenni, R. A., et al. (2014). Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc. Natl. Acad. Sci. U.S.A. 111, 12883-12888. doi: 10.1073/pnas.1410551111
94. Pitts, K. E., Dobbin, P. S., Reyes-Ramirez, F., Thomson, A. J., Richardson, D. J., and Seward, H. E. (2003). Characterization of the Shewanella oneidensis MR-1 decaheme cytochrome MtrA: expression in Escherichia coli confers the ability to reduce soluble Fe(III) chelates. J. Biol. Chem. 278, 27758-27765. doi: 10.1074/jbc.M302582200
95. Poehlein, A., Schmidt, S., Kaster, A.-K., Goenrich, M., Vollmers, J., Thürmer, A., et al. (2012). An ancient pathway combining carbon dioxide fixation with the generation and utilization of a sodium ion gradient for ATP synthesis. PLoS ONE 7:e33439. doi: 10.1371/journal.pone.0033439
96. Potter, M. C. (1911). Electrical effects accompanying the decomposition of organic compounds. Proc. R. Soc. Lond. B 1911, 260-276. doi: 10.1098/rspb.1911.0073
97. Qian, X., Mester, T., Morgado, L., Arakawa, T., Sharma, M. L., Inoue, K., et al. (2011). Biochemical characterization of purified OmcS, a c-type cytochrome required for insoluble Fe (III) reduction in Geobacter sulfurreducens. Biochim. Biophys. Acta 1807, 404-412. doi: 10.1016/j.bbabio.2011.01.003
98. Qiao, Y., Li, C. M., Bao, S.-J., Lu, Z., and Hong, Y. (2008). Direct electrochemistry and electrocatalytic mechanism of evolved Escherichia coli cells in microbial fuel cells. Chem. Commun. 11, 1290-1292. doi: 10.1039/b719955d
99. Rabaey, K., Boon, N., Höfte, M., and Verstraete, W. (2005). Microbial phenazine production enhances electron transfer in biofuel cells. Environ. Sci. Technol. 39, 3401-3408. doi: 10.1021/es048563o
100. Rabaey, K., Boon, N., Siciliano, S. D., Verhaege, M., and Verstraete, W. (2004). Biofuel cells select for microbial consortia that self-mediate electron transfer. Appl. Environ. Microbiol. 70, 5373-5382. doi: 10.1128/AEM.70.9.5373-5382.2004
101. Rabaey, K., and Rozendal, R. A. (2010). Microbial electrosynthesis-revisiting the electrical route for microbial production. Nat. Rev. Microbiol. 8, 706-716. doi: 10.1038/nrmicro2422
102. Ragsdale, S. W., and Pierce, E. (2008). Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochim. Biophys. Acta 1784, 1873-1898. doi: 10.1016/j.bbapap.2008.08.012
103. Reguera, G., Nevin, K. P., Nicoll, J. S., Covalla, S. F., Woodard, T. L., and Lovley, D. R. (2006). Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl. Environ. Microbiol. 72, 7345-7348. doi: 10.1128/AEM.01444-06
104. Richardson, D. J., Edwards, M. J., White, G. F., Baiden, N., Hartshorne, R. S., Fredrickson, J. K., et al. (2012). Exploring the biochemistry at the extracellular redox frontier of bacterial mineral Fe (III) respiration. Biochem. Soc. Trans. 40, 493-500. doi: 10.1042/BST20120018
105. Richter, H., Nevin, K. P., Jia, H., Lowy, D. A., Lovley, D. R., and Tender, L. M. (2009). 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. doi: 10.1039/b816647a
106. Richter, K., Schicklberger, M., and Gescher, J. (2012). Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Appl. Environ. Microbiol. 78, 913-921. doi: 10.1128/AEM.06803-11
107. Rosenbaum, M., Aulenta, F., Villano, M., and Angenent, L. T. (2011). Cathodes as electron donors for microbial metabolism: which extracellular electron transfer mechanisms are involved? Bioresour. Technol. 102, 324-333. doi: 10.1016/j.biortech.2010.07.008
108. Ross, D. E., Flynn, J. M., Baron, D. B., Gralnick, J. A., and Bond, D. R. (2011). Towards electrosynthesis in Shewanella: energetics of reversing the Mtr pathway for reductive metabolism. PLoS ONE 6:e16649. doi: 10.1371/journal.pone.0016649
109. Sasaki, K., Tsuge, Y., Sasaki, D., and Kondo, A. (2014). Increase in lactate yield by growing Corynebacterium glutamicum in a bioelectrochemical reactor. J. Biosci. Bioeng. 117, 598-601. doi: 10.1016/j.jbiosc.2013.10.026
110. Schiel-Bengelsdorf, B., and Dürre, P. (2012). Pathway engineering and synthetic biology using acetogens. FEBS Lett. 586, 2191-2198. doi: 10.1016/j.febslet.2012.04.043
111. Schröder, U., Nießen, J., and Scholz, F. (2003). A generation of microbial fuel cells with current outputs boosted by more than one order of magnitude. Angew. Chem. Int. Ed. 42, 2880-2883. doi: 10.1002/anie.200350918
112. Schrott, G. D., Bonanni, P. S., Robuschi, L., Esteve-Nuñez, A., and Busalmen, J. P. (2011). Electrochemical insight into the mechanism of electron transport in biofilms of Geobacter sulfurreducens. Electrochim. Acta 56, 10791-10795. doi: 10.1016/j.electacta.2011.07.001
113. Schuchmann, K., and Müller, V. (2012). A bacterial electron-bifurcating hydrogenase. J. Biol. Chem. 287, 31165-31171. doi: 10.1074/jbc.M112.395038
114. Schuchmann, K., and Müller, V. (2014). Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat. Rev. Microbiol. 12, 809-821. doi: 10.1038/nrmicro3365
115. Shi, L., Richardson, D. J., Wang, Z., Kerisit, S. N., Rosso, K. M., Zachara, J. M., et al. (2009). The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ. Microbiol. Rep. 1, 220-227. doi: 10.1111/j.1758-2229.2009.00035.x
116. Shi, L., Rosso, K., Zachara, J., and Fredrickson, J. (2012). Mtr extracellular electron-transfer pathways in Fe (III)-reducing or Fe (II)-oxidizing bacteria: a genomic perspective. Biochem. Soc. Trans. 40, 1261-1267. doi: 10.1042/BST20120098
117. Shi, L., Squier, T. C., Zachara, J. M., and Fredrickson, J. K. (2007). Respiration of metal (hydr) oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol. Microbiol. 65, 12-20. doi: 10.1111/j.1365-2958.2007.05783.x
118. Shin, H., Zeikus, J., and Jain, M. (2002). Electrically enhanced ethanol fermentation by Clostridium thermocellum and Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 58, 476-481. doi: 10.1007/s00253-001-0923-2
119. Shirodkar, S., Reed, S., Romine, M., and Saffarini, D. (2011). The octahaem SirA catalyses dissimilatory sulfite reduction in Shewanella oneidensis MR-1. Environ. Microbiol. 13, 108-115. doi: 10.1111/j.1462-2920.2010.02313.x
120. Simpson, P. J., Richardson, D. J., and Codd, R. (2010). The periplasmic nitrate reductase in Shewanella: the resolution, distribution and functional implications of two NAP isoforms, NapEDABC and NapDAGHB. Microbiology 156, 302-312. doi: 10.1099/mic.0.034421-0
121. Steinbusch, K. J., Hamelers, H. V., Schaap, J. D., Kampman, C., and Buisman, C. J. (2009). Bioelectrochemical ethanol production through mediated acetate reduction by mixed cultures. Environ. Sci. Technol. 44, 513-517. doi: 10.1021/es902371e
122. Straub, K. L., Benz, M., and Schink, B. (2001). Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiol. Ecol. 34, 181-186. doi: 10.1111/j.1574-6941.2001.tb00768.x
123. Strycharz, S. M., Glaven, R. H., Coppi, M. V., Gannon, S. M., Perpetua, L. A., Liu, A., et al. (2011). Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens. Bioelectrochemistry 80, 142-150. doi: 10.1016/j.bioelechem.2010.07.005
124. Strycharz, S. M., Woodard, T. L., Johnson, J. P., Nevin, K. P., Sanford, R. A., Löffler, F. E., et al. (2008). Graphite electrode as a sole electron donor for reductive dechlorination of tetrachlorethene by Geobacter lovleyi. Appl. Environ. Microbiol. 74, 5943-5947. doi: 10.1128/AEM.00961-08
125. Strycharz-Glaven, S. M., and Tender, L. M. (2012). 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. Energy Environ. Sci. 5, 6250-6255. doi: 10.1039/c2ee02613a.
126. Sydow, A., Krieg, T., Mayer, F., Schrader, J., and Holtmann, D. (2014). Electroactive bacteria-molecular mechanisms and genetic tools. Appl. Microbiol. Biotechnol. 98, 8481-8495. doi: 10.1007/s00253-014-6005-z
127. Tatsumi, N., and Inui, M. (2012). Corynebacterium glutamicum: Biology and Biotechnology. Heidelberg: Springer Science & Business Media.
128. TerAvest, M. A., Zajdel, T. J., and Ajo-Franklin, C. M. (2014). The Mtr pathway of Shewanella oneidensis MR-1 couples substrate utilization to current production in Escherichia coli. ChemElectroChem 1, 1874-1879. doi: 10.1002/celc.201402194
129. Thamdrup, B. (2000). Bacterial manganese and iron reduction in aquatic sediments. Adv. Microb. Ecol. 16, 41-84. doi: 10.1007/978-1-4615-4187-5_2
130. Thrash, J. C., and Coates, J. D. (2008). Review: direct and indirect electrical stimulation of microbial metabolism. Environ. Sci. Technol. 42, 3921-3931. doi: 10.1021/es702668w
131. Tracy, B. P., Jones, S. W., Fast, A. G., Indurthi, D. C., and Papoutsakis, E. T. (2012). Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications. Curr. Opin. Biotechnol. 23, 364-381. doi: 10.1016/j.copbio.2011.10.008
132. Tremblay, P.-L., and Zhang, T. (2015). Electrifying microbes for the production of chemicals. Front. Microbiol. 6:201. doi: 10.3389/fmicb.2015.00201
133. Tremblay, P.-L., Zhang, T., Dar, S. A., Leang, C., and Lovley, D. R. (2013). The Rnf complex of Clostridium ljungdahlii is a proton-translocating ferredoxin: NAD+ oxidoreductase essential for autotrophic growth. MBio 4, e00406-e00412.
134. Unden, G., and Bongaerts, J. (1997). Alternative respiratory pathways of Escherischia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim. Biophys. Acta 1320, 217-234. doi: 10.1016/S0005-2728(97)00034-0
135. Vignais, P. M., and Billoud, B. (2007). Occurrence, classification, and biological function of hydrogenases: an overview. Chem. Rev. 107, 4206-4272. doi: 10.1021/cr050196r
136. Vijgenboom, E., Busch, J. E., and Canters, G. W. (1997). In vivo studies disprove an obligatory role of azurin in denitrification in Pseudomonas aeruginosa and show that azu expression is under control of RpoS and ANR. Microbiology 143, 2853-2863. doi: 10.1099/00221287-143-9-2853
137. Wagner, R. C., Regan, J. M., Oh, S.-E., Zuo, Y., and Logan, B. E. (2009). Hydrogen and methane production from swine wastewater using microbial electrolysis cells. Water Res. 43, 1480-1488. doi: 10.1016/j.watres.2008.12.037
138. Wang, S., Huang, H., Kahnt, J., and Thauer, R. K. (2013). A reversible electron-bifurcating ferredoxin-and NAD-dependent [FeFe]-hydrogenase (HydABC) in Moorella thermoacetica. J. Bacteriol. 195, 1267-1275. doi: 10.1128/JB.02158-12
139. Welte, C., Krätzer, C., and Deppenmeier, U. (2010). Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei. FEBS J. 277, 3396-3403. doi: 10.1111/j.1742-4658.2010.07744.x
140. White, G. F., Shi, Z., Shi, L., Wang, Z., Dohnalkova, A. C., Marshall, M. J., et al. (2013). Rapid electron exchange between surface-exposed bacterial cytochromes and Fe (III) minerals. Proc. Natl. Acad. Sci. U.S.A. 110, 6346-6351. doi: 10.1073/pnas.1220074110
141. Williams, K. H., Nevin, K. P., Franks, A., Englert, A., Long, P. E., and Lovley, D. R. (2009). Electrode-based approach for monitoring in situ microbial activity during subsurface bioremediation. Environ. Sci. Technol. 44, 47-54. doi: 10.1021/es9017464
142. Wrighton, K. C., Thrash, J. C., Melnyk, R. A., Bigi, J. P., Byrne-Bailey, K. G., Remis, J. P., et al. (2011). Evidence for direct electron transfer by a gram-positive bacterium isolated from a microbial fuel cell. Appl. Environ. Microbiol. 77, 7633-7639. doi: 10.1128/aem.05365-11
143. Yang, Y., Ding, Y., Hu, Y., Cao, B., Rice, S. A., Kjelleberg, S., et al. (2015). Enhancing bidirectional electron transfer of Shewanella oneidensis by a synthetic flavin pathway. ACS Synth. Biol. doi: 10.1021/sb500331x [Epub ahead of print].
144. Yang, Y., Xu, M., Guo, J., and Sun, G. (2012). Bacterial extracellular electron transfer in bioelectrochemical systems. Process Biochem. 47, 1707-1714. doi: 10.1016/j.procbio.2012.07.032
145. Zhang, T., Cui, C., Chen, S., Ai, X., Yang, H., Shen, P., et al. (2006). A novel mediatorless microbial fuel cell based on direct biocatalysis of Escherichia coli. Chem. Commun. 21, 2257-2259. doi: 10.1039/b600876c
146. Zhang, T., Gannon, S. M., Nevin, K. P., Franks, A. E., and Lovley, D. R. (2010). Stimulating the anaerobic degradation of aromatic hydrocarbons in contaminated sediments by providing an electrode as the electron acceptor. Environ. Microbiol. 12, 1011-1020. doi: 10.1111/j.1462-2920.2009.02145.x
147. Zhang, T., Zeng, Y., Chen, S., Ai, X., and Yang, H. (2007). Improved performances of E. coli catalyzed microbial fuel cells with composite graphite/PTFE anodes. Electrochem. Commun. 9, 349-353. doi: 10.1016/j.elecom.2006.09.025