Extracellular Electron Uptake: Among Autotrophs and Mediated by Surfaces

Trends in Biotechnology

Volumn 35, Issue 4, 2017, Pages 360-371

  Tremblay, Pier Luc ^a,b   Angenent, Largus T ^c,d   Zhang, Tian ^a,b  

^a WUHAN UNIVERSITY OF TECHNOLOGY   (China)

^b Chalmers University of Technology   (Denmark)

^c Department of Obstetrics Gynecology   (United States)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

biocorrosion; extracellular electron transfer; interspecies electron transfer; microbial electrosynthesis

Indexed keywords

BACTERIA; BIODEGRADATION; CARBON DIOXIDE; CORROSION; ELECTRODES; ELECTRON TRANSITIONS; ENZYME ELECTRODES; GREENHOUSE GASES; MICROORGANISMS; WASTEWATER TREATMENT;

BIOCORROSION; ELECTRON TRANSFER; ELECTRON TRANSFER PROTEINS; ENERGETIC EFFICIENCY; EXTRACELLULAR ELECTRON TRANSFER; MICROBIAL ELECTROSYNTHESIS; MICROBIALLY INFLUENCED CORROSION; VALUE ADDED PRODUCTS;

ELECTRONS;

ACTIVATED CARBON; AMMONIA; CARBON DIOXIDE; CYTOCHROME; FORMATE DEHYDROGENASE; FORMIC ACID; HEME; HYDROGEN; IRON; MAGNETITE;

ANAEROBIC DIGESTION; AUTOTROPH; BACTERIAL OUTER MEMBRANE; BIOGEOCHEMICAL CYCLE; BIOSYNTHESIS; CATALYST; CELL COMPONENT; CELL DEATH; ELECTRODE; ELECTRON TRANSPORT; GREENHOUSE GAS; METHANOGEN; MICROBIAL CORROSION; MICROBIAL ELECTROSYNTHESIS; MICROBIAL METABOLISM; NONHUMAN; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; AUTOTROPHY; BACTERIUM; BIOREACTOR; CHEMISTRY; ELECTROCHEMICAL ANALYSIS; ELECTRON; EXTRACELLULAR SPACE; METABOLISM; MICROBIOLOGY; SURFACE PROPERTY;

AUTOTROPHIC PROCESSES; BACTERIA; BIOREACTORS; CARBON DIOXIDE; ELECTROCHEMICAL TECHNIQUES; ELECTRONS; EXTRACELLULAR SPACE; HYDROGEN; SURFACE PROPERTIES;

EID: 85005917697     PISSN: 01677799     EISSN: 18793096     Source Type: Journal    
DOI: 10.1016/j.tibtech.2016.10.004     Document Type: Review

References (92)

1. 1 Shrestha, P.M., Rotaru, A.-E., Plugging in or going wireless: strategies for interspecies electron transfer. Front. Microbiol., 5, 2014, 237.
2. 2 Kouzuma, A., et al. Microbial interspecies interactions: recent findings in syntrophic consortia. Front. Microbiol., 13, 2015, 477.
3. 3 Usher, K.M., et al. Critical review: microbially influenced corrosion of buried carbon steel pipes. Int. Biodeterior. Biodegradation 93 (2014), 84–106.
4. 4 Koch, G.H., et al. Corrosion Cost and Preventive Strategies in the United States. 2002, Federal Highway Administration.
5. 5 Schink, B., Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 61 (1997), 262–280.
6. 6 McInerney, M.J., et al. Syntrophy in anaerobic global carbon cycles. Curr. Opin. Biotechnol. 20 (2009), 623–632.
7. 7 Kato, S., et al. Isolation of acetogenic bacteria that induce biocorrosion by utilizing metallic iron as the sole electron donor. Appl. Environ. Microbiol. 81 (2015), 67–73.
8. 8 Lovley, D.R., Nevin, K.P., Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity. Curr. Opin. Biotechnol. 24 (2013), 385–390.
9. 9 Rabaey, K., Rozendal, R.A., Microbial electrosynthesis – revisiting the electrical route for microbial production. Nat. Rev. Microbiol. 8 (2010), 706–716.
10. 10 Cheng, S., et al. Direct biological conversion of electrical current into methane by electromethanogenesis. Environ. Sci. Technol. 43 (2009), 3953–3958.
11. 4 via direct and indirect extracellular electron transfer by a hydrogenophilic methanogenic culture. Bioresour. Technol. 101 (2010), 3085–3090.
12. 12 Nevin, K.P., et al. Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. MBio 1 (2010), e00103–e00110.
13. 2 fixation by Fe(II)-oxidizing bacteria coupled with direct uptake of electrons from solid electron sources. Front. Microbiol., 6, 2015, 994.
14. 14 Doud, D.F.R., Angenent, L.T., Toward electrosynthesis with uncoupled extracellular electron uptake and metabolic growth: enhancing current uptake with Rhodopseudomonas palustris. Environ. Sci. Technol. Lett. 1 (2014), 351–355.
15. 15 Khunjar, W.O., et al. Biomass production from electricity using ammonia as an electron carrier in a reverse microbial fuel cell. PLoS One, 7, 2012, e44846.
16. 16 Marshall, C.W., et al. Electrosynthesis of commodity chemicals by an autotrophic microbial community. Appl. Environ. Microbiol. 78 (2012), 8412–8420.
17. 2 to higher alcohols. Science, 335, 2012, 1596.
18. 18 Rosenbaum, M., et al. Cathodes as electron donors for microbial metabolism: which extracellular electron transfer mechanisms are involved?. Bioresour. Technol. 102 (2011), 324–333.
19. 2 reduction. Energy Environ. Sci. 8 (2015), 3731–3744.
20. 20 Aulenta, F., et al. Kinetics of trichloroethene dechlorination and methane formation by a mixed anaerobic culture in a bio-electrochemical system. Electrochim. Acta 53 (2008), 5300–5305.
21. 21 DuBois, D.L., Electrochemical reactions of carbon dioxide. Encyclopedia of Electrochemistry, vol. 7A, 2007, Wiley-VCH, 202–225.
22. 22 Deutzmann, J.S., et al. Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis. MBio 6 (2015), e00496–e00515.
23. 23 Bose, A., et al. Electron uptake by iron-oxidizing phototrophic bacteria. Nat. Commun., 5, 2014, 3391.
24. 24 Beese-Vasbender, P.F., et al. Selective microbial electrosynthesis of methane by a pure culture of a marine lithoautotrophic archaeon. Bioelectrochemistry 102 (2015), 50–55.
25. 25 Mohanakrishna, G., et al. An enriched electroactive homoacetogenic biocathode for the microbial electrosynthesis of acetate through carbon dioxide reduction. Faraday Discuss. 183 (2015), 445–462.
26. 26 Summers, Z.M., et al. Cultivation of an obligate Fe(II)-oxidizing lithoautotrophic bacterium using electrodes. MBio, 4, 2013 e00420-412.
27. 27 Carbajosa, S., et al. Electrochemical growth of Acidithiobacillus ferrooxidans on a graphite electrode for obtaining a biocathode for direct electrocatalytic reduction of oxygen. Biosens. Bioelectron. 26 (2010), 877–880.
28. 2 catalysed by Geobacter sulfurreducens grown on polarized stainless steel cathodes. Electrochem. Commun. 28 (2013), 27–30.
29. 29 Gregory, K.B., et al. Graphite electrodes as electron donors for anaerobic respiration. Environ. Microbiol. 6 (2004), 596–604.
30. 30 Gregory, K.B., Lovley, D.R., Remediation and recovery of uranium from contaminated subsurface environments with electrodes. Environ. Sci. Technol. 39 (2005), 8943–8947.
31. 31 Mori, K., et al. Iron corrosion activity of anaerobic hydrogen-consuming microorganisms isolated from oil facilities. J. Biosci. Bioeng. 110 (2010), 426–430.
32. 32 Dinh, H.T., et al. Iron corrosion by novel anaerobic microorganisms. Nature 427 (2004), 829–832.
33. 33 Venzlaff, H., et al. Accelerated cathodic reaction in microbial corrosion of iron due to direct electron uptake by sulfate-reducing bacteria. Corros. Sci. 66 (2013), 88–96.
34. 34 Deng, X., et al. Electron extraction from an extracellular electrode by Desulfovibrio ferrophilus strain IS5 without using hydrogen as an electron carrier. Electrochemistry 83 (2015), 529–531.
35. 35 Uchiyama, T., et al. Iron-corroding methanogen isolated from a crude-oil storage tank. Appl. Environ. Microbiol. 76 (2010), 1783–1788.
36. 36 Dowling, N.J.E., et al. Effects of selection and fate of substrates supplied to anaerobic bacteria involved in the corrosion of pipe-line steel. J. Ind. Microbiol. 10 (1992), 207–215.
37. 37 Pisciotta, J.M., et al. Enrichment of microbial electrolysis cell biocathodes from sediment microbial fuel cell bioanodes. Appl. Environ. Microbiol. 78 (2012), 5212–5219.
38. 38 Iino, T., et al. Iron corrosion induced by nonhydrogenotrophic nitrate-reducing Prolixibacter sp. strain MIC1-1. Appl. Environ. Microbiol. 81 (2015), 1839–1846.
39. 39 Iino, T., et al. Prolixibacter denitrificans sp. nov., an iron-corroding, facultatively aerobic, nitrate-reducing bacterium isolated from crude oil, and emended descriptions of the genus Prolixibacter and Prolixibacter bellariivorans. Int. J. Syst. Evol. Microbiol. 65 (2015), 2865–2869.
40. 40 Sieber, J.R., et al. The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism. Environ. Microbiol. 16 (2014), 177–188.
41. 41 Smith, J.A., et al. Syntrophic growth via quinone-mediated interspecies electron transfer. Front. Microbiol., 6, 2015, 121.
42. 42 Milucka, J., et al. Zero-valent sulphur is a key intermediate in marine methane oxidation. Nature 491 (2012), 541–546.
43. 43 Kaden, J., et al. Cysteine-mediated electron transfer in syntrophic acetate oxidation by cocultures of Geobacter sulfurreducens and Wolinella succinogenes. Arch. Microbiol. 178 (2002), 53–58.
44. 44 Summers, Z.M., et al. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330 (2010), 1413–1415.
45. 45 Rotaru, A.-E., et al. A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ. Sci. 7 (2014), 408–415.
46. 46 Malvankar, N.S., et al. Structural basis for metallic-like conductivity in microbial nanowires. MBio, 6, 2015, e00084.
47. 47 Malvankar, N.S., et al. Tunable metallic-like conductivity in microbial nanowire networks. Nat. Nanotechnol. 6 (2011), 573–579.
48. 48 Vargas, M., et al. Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. MBio 4 (2013), e00105–e00113.
49. 49 Lampa-Pastirk, S., et al. Thermally activated charge transport in microbial protein nanowires. Sci. Rep., 6, 2016, 23517.
50. 50 Feliciano, G.T., et al. Structural and functional insights into the conductive pili of Geobacter sulfurreducens revealed in molecular dynamics simulations. Phys. Chem. Chem. Phys. 17 (2015), 22217–22226.
51. 51 Yates, M.D., et al. Thermally activated long range electron transport in living biofilms. Phys. Chem. Chem. Phys. 17 (2015), 32564–32570.
52. 52 Snider, R.M., et al. Long-range electron transport in Geobacter sulfurreducens biofilms is redox gradient-driven. Proc. Natl Acad. Sci. U.S.A. 109 (2012), 15467–15472.
53. 53 Ordóñez, M.V., et al. The relay network of Geobacter biofilms. Energy Environ. Sci. 9 (2016), 2677–2681.
54. 54 Strycharz, S.M., et al. Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens. Bioelectrochemistry 80 (2011), 142–150.
55. 55 Smith, J.A., et al. Outer cell surface components essential for Fe(III) oxide reduction by Geobacter metallireducens. Appl. Environ. Microbiol. 79 (2013), 901–907.
56. 56 Leang, C., et al. Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. Appl. Environ. Microbiol. 76 (2010), 4080–4084.
57. 2): an innovative method for biogas upgrading. Bioresour. Technol. 173 (2014), 392–398.
58. 58 McGlynn, S.E., et al. Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature 526 (2015), 531–535.
59. 59 Wegener, G., et al. Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria. Nature 526 (2015), 587–590.
60. 60 Byrne, J.M., et al. Redox cycling of Fe(II) and Fe(III) in magnetite by Fe-metabolizing bacteria. Science 347 (2015), 1473–1476.
61. 61 Liu, F., et al. Magnetite compensates for the lack of a pilin-associated c-type cytochrome in extracellular electron exchange. Environ. Microbiol. 17 (2015), 648–655.
62. 62 Liu, F., et al. Promoting direct interspecies electron transfer with activated carbon. Energy Environ. Sci. 5 (2012), 8982–8989.
63. 63 Kato, S., et al. Microbial interspecies electron transfer via electric currents through conductive minerals. Proc. Natl Acad. Sci. U.S.A. 109 (2012), 10042–10046.
64. 64 Jiang, S., et al. Methanogenesis facilitated by geobiochemical iron cycle in a novel syntrophic methanogenic microbial community. Environ. Sci. Technol. 47 (2013), 10078–10084.
65. 65 Yamada, C., et al. Conductive iron oxides accelerate thermophilic methanogenesis from acetate and propionate. J. Biosci. Bioeng. 119 (2015), 678–682.
66. 66 Li, H., et al. Direct interspecies electron transfer accelerates syntrophic oxidation of butyrate in paddy soil enrichments. Environ. Microbiol. 17 (2015), 1533–1547.
67. 67 De Vrieze, J., et al. Biomass retention on electrodes rather than electrical current enhances stability in anaerobic digestion. Water Res. 54 (2014), 211–221.
68. 68 Cruz Viggi, C., et al. Magnetite particles triggering a faster and more robust syntrophic pathway of methanogenic propionate degradation. Environ. Sci. Technol. 48 (2014), 7536–7543.
69. 2 to organic products. Sci. Rep., 5, 2015, 16168.
70. 70 de Campos Rodrigues, T., Rosenbaum, M.A., Microbial electroreduction: screening for new cathodic biocatalysts. ChemElectroChem 1 (2014), 1916–1922.
71. 71 Tremblay, P.-L., Zhang, T., Electrifying microbes for the production of chemicals. Front. Microbiol., 6, 2015, 201.
72. 2 by a highly structured biofilm assembled with reduced graphene oxide–tetraethylene pentamine. J. Mater. Chem. A 4 (2016), 8395–8401.
73. 73 Jourdin, L., et al. Biologically induced hydrogen production drives high rate/high efficiency microbial electrosynthesis of acetate from carbon dioxide. ChemElectroChem 3 (2016), 581–591.
74. 74 Villano, M., et al. Carbon and nitrogen removal and enhanced methane production in a microbial electrolysis cell. Bioresour. Technol. 130 (2013), 366–371.
75. 75 Jürgensen, L., et al. Utilization of surplus electricity from wind power for dynamic biogas upgrading: Northern Germany case study. Biomass Bioenerg. 66 (2014), 126–132.
76. 76 Giddings, C.G.S., et al. Simplifying microbial electrosynthesis reactor design. Front. Microbiol., 6, 2015, 468.
77. 77 Luo, X., et al. Methane production in microbial reverse-electrodialysis methanogenesis cells (MRMCs) using thermolytic solutions. Environ. Sci. Technol. 48 (2014), 8911–8918.
78. 78 Andersen, S.J., et al. Electrolytic membrane extraction enables production of fine chemicals from biorefinery sidestreams. Environ. Sci. Technol. 48 (2014), 7135–7142.
79. 2 through microbial electrosynthesis. Environ. Sci. Technol. Lett. 2 (2015), 325–328.
80. 80 Xu, J., et al. In-line and selective phase separation of medium-chain carboxylic acids using membrane electrolysis. Chem. Commun. 51 (2015), 6847–6850.
81. 81 Nichols, E.M., et al. Hybrid bioinorganic approach to solar-to-chemical conversion. Proc. Natl Acad. Sci. U.S.A. 112 (2015), 11461–11466.
82. 82 Liu, C., et al. Nanowire-bacteria hybrids for unassisted solar carbon dioxide fixation to value-added chemicals. Nano Lett. 15 (2015), 3634–3639.
83. 83 Torella, J.P., et al. Efficient solar-to-fuels production from a hybrid microbial–water-splitting catalyst system. Proc. Natl Acad. Sci. U.S.A. 112 (2015), 2337–2342.
84. 2 reduction efficiencies exceeding photosynthesis. Science 352 (2016), 1210–1213.
85. 85 Zhang, T., More efficient together. Science 350 (2015), 738–739.
86. 86 Menezes, A.A., et al. Towards synthetic biological approaches to resource utilization on space missions. J. R. Soc. Interface, 12, 2015, 20140715.
87. 87 Bajracharya, S., et al. Carbon dioxide reduction by mixed and pure cultures in microbial electrosynthesis using an assembly of graphite felt and stainless steel as a cathode. Bioresour. Technol. 195 (2015), 14–24.
88. 2 to multi-carbon chemicals with a mixed culture avoiding methanogenesis. Bioelectrochemistry 113 (2017), 26–34.
89. 89 Zeppilli, M., et al. Effect of the anode feeding composition on the performance of a continuous-flow methane-producing microbial electrolysis cell. Environ. Sci. Pollut. Res. Int. 22 (2015), 7349–7360.
90. 90 LaBelle, E.V., et al. Influence of acidic pH on hydrogen and acetate production by an electrosynthetic microbiome. PLoS One, 9, 2014, e109935.
91. 91 Ueki, T., et al. Converting carbon dioxide to butyrate with an engineered strain of Clostridium ljungdahlii. MBio, 5, 2014 e01636-1614.
92. 92 Jourdin, L., et al. High acetic acid production rate obtained by microbial electrosynthesis from carbon dioxide. Environ. Sci. Technol. 49 (2015), 13566–13574.