Microbial Conversion of Carbon Dioxide to Electrofuels

  • Jongoh Shin
  • Yoseb Song
  • Sangrak Jin
  • Suhyung Cho
  • Byung-Kwan Cho
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Electrofuel produced by microbes utilizing CO2 and electricity as carbon and energy sources, respectively, has received much attention as an alternative to fossil fuels. Based on the inherent capabilities of microorganisms, extracellular electron transfer (EET) was demonstrated with various modes of cathodic electron transfer. With extensive studies on Geobacter sulfurreducens and Shewanella oneidensis, it was confirmed that cytochromes located in the outer membrane are essential for direct EET. Although a few electroactive bacteria are cytochrome independent, key compounds potentially involved in EET can be determined based on their redox functions, which were successfully demonstrated in electroactive acetogens and Ralstonia eutropha. Electroactive acetogens reduce CO2 with electric power at the cathode and direct sunlight with a self-photosensitized nanoparticle for the production of organic compounds. Furthermore, a hybrid water splitting-biosynthetic system, which consists of advanced catalysts and genetically modified R. eutropha, exhibited production of diverse electrofuels with high CO2 reduction efficiency. To improve the production of electrofuels, basic research and engineering of microorganisms and modification of electrodes is essential.

Keywords

Biomass TiO2 Cadmium Respiration Pyruvate 

References

  1. Badger MR, Bek EJ (2008) Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J Exp Bot 59(7):1525–1541CrossRefPubMedGoogle Scholar
  2. Bowien B, Kusian B (2002) Genetics and control of CO(2) assimilation in the chemoautotroph Ralstonia eutropha. Arch Microbiol 178(2):85–93CrossRefPubMedGoogle Scholar
  3. Bretschger O, Obraztsova A, Sturm CA, Chang IS, Gorby YA, Reed SB, Culley DE, Reardon CL, Barua S, Romine MF, Zhou J, Beliaev AS, Bouhenni R, Saffarini D, Mansfeld F, Kim B-H, Fredrickson JK, Nealson KH (2007) Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl Environ Microbiol 73(21):7003–7012CrossRefPubMedPubMedCentralGoogle Scholar
  4. Brigham CJ, Gai CS, Lu J, Speth DR, Worden RM, Sinskey AJ (2012) Chapter 39: Engineering Ralstonia eutropha for production of isobutanol from CO2, H2, and O2. In: Advanced biofuels and bioproducts. Springer, New YorkGoogle Scholar
  5. Cheng S, Xing D, Call DF, Logan BE (2009) Direct biological conversion of electrical current into methane by electromethanogenesis. Environ Sci Technol 43(10):3953–3958CrossRefPubMedGoogle Scholar
  6. Cramm R (2009) Genomic view of energy metabolism in Ralstonia eutropha H16. J Mol Microbiol Biotechnol 16(1–2):38–52CrossRefPubMedGoogle Scholar
  7. Deutzmann JS, Sahin M, Spormann AM (2015) Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis. MBio 6(2):1CrossRefGoogle Scholar
  8. Drake HL (1994) Chapter 1: Acetogenesis, acetogenic bacteria, and the acetyl-CoA “Wood/Ljungdahl” pathway: past and current perspectives. In: Acetogenesis. One Penn Plaza, New York, NY 10119: Springer USGoogle Scholar
  9. Drake HL, Gößner AS, Daniel SL (2008) Old acetogens, new light. Ann N Y Acad Sci 1125:100–128CrossRefPubMedGoogle Scholar
  10. Fast AG, Papoutsakis ET (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(4):380–395CrossRefGoogle Scholar
  11. Gottwald M, Andreesen JR, LeGall J, Ljungdahl LG (1975) Presence of cytochrome and menaquinone in Clostridium formicoaceticum and Clostridium thermoaceticum. J Bacteriol 122(1):325–328PubMedPubMedCentralGoogle Scholar
  12. Gregory KB, Bond DR, Lovley DR (2004) Graphite electrodes as electron donors for anaerobic respiration. Environ Microbiol 6 (6):596–604CrossRefPubMedGoogle Scholar
  13. Hernandez ME, Newman DK (2001) Extracellular electron transfer. Cell Mol Life Sci 58(11):1562–1571CrossRefPubMedGoogle Scholar
  14. Hou Y, Abrams BL, Vesborg PCK, Björketun ME, Herbst K, Bech L, Setti AM, Damsgaard CD, Pedersen T, Hansen O, Rossmeisl J, Dahl S, Nørskov JK, Chorkendorff I (2011) Bioinspired molecular co-catalysts bonded to a silicon photocathode for solar hydrogen evolution. Nat Mater 10(6):434–438CrossRefPubMedGoogle Scholar
  15. Huang H, Wang S, Moll J, Thauer RK (2012) Electron bifurcation involved in the energy metabolism of the acetogenic bacterium Moorella thermoacetica growing on glucose or H2 plus CO2. J Bacteriol 194(14):3689–3699CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ikeda S, Takagi T, Ito K (1987) Selective formation of formic acid, oxalic acid, and carbon monoxide by electrochemical reduction of carbon dioxide. BCSJ 60(7):2517–2522CrossRefGoogle Scholar
  17. Köpke M, Held C, Hujer S, Liesegang H, Wiezer A, Wollherr A, Ehrenreich A, Liebl W, Gottschalk G, Dürre P (2010) Clostridium ljungdahlii represents a microbial production platform based on syngas. Proc Natl Acad Sci U S A 107(29):13087–13092CrossRefPubMedPubMedCentralGoogle Scholar
  18. Köpke M, Mihalcea C, Liew F, Tizard JH, Ali MS, Conolly JJ, Al-Sinawi B, Simpson SD (2011) 2,3-butanediol production by acetogenic bacteria, an alternative route to chemical synthesis, using industrial waste gas. Appl Environ Microbiol 77(15):5467–5475CrossRefPubMedPubMedCentralGoogle Scholar
  19. Kracke F, Vassilev I, Krömer JO (2015) Microbial electron transport and energy conservation – the foundation for optimizing bioelectrochemical systems. Front Microbiol 6:575CrossRefPubMedPubMedCentralGoogle Scholar
  20. Leang C, Ueki T, Nevin KP, Lovley DR (2013) A genetic system for Clostridium ljungdahlii: a chassis for autotrophic production of biocommodities and a model homoacetogen. Appl Environ Microbiol 79(4):1102–1109CrossRefPubMedPubMedCentralGoogle Scholar
  21. Li H, Opgenorth PH, Wernick DG, Rogers S, Wu T-Y, Higashide W, Malati P, Huo Y-X, Cho KM, Liao JC (2012) Integrated electromicrobial conversion of CO2 to higher alcohols. Science 335(6076):1596–1596CrossRefPubMedGoogle Scholar
  22. Liu C, Colón BC, Ziesack M, Silver PA, Nocera DG (2016) Water splitting-biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis. Science 352(6290):1210–1213CrossRefPubMedGoogle Scholar
  23. Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan KA, Aklujkar M, Butler JE, Giloteaux L, Rotaru A-E, Holmes DE, Franks AE, Orellana R, Risso C, Nevin KP (2011) Geobacter: the microbe electric’s physiology, ecology, and practical applications. Adv Microb Physiol 59:1–100CrossRefPubMedGoogle Scholar
  24. Lu J, Brigham CJ, Gai CS, Sinskey AJ (2012) Studies on the production of branched-chain alcohols in engineered Ralstonia eutropha. Appl Microbiol Biotechnol 96(1):283–297CrossRefPubMedGoogle Scholar
  25. Lu J, Brigham CJ, Li S, Sinskey AJ (2016) Ralstonia eutropha H16 as a platform for the production of biofuels, biodegradable plastics, and fine chemicals from diverse carbon resources. In: Biotechnology for biofuel production and optimization. Elsevier, Amsterdam, pp 325–351Google Scholar
  26. Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A 105(10):3968–3973CrossRefPubMedPubMedCentralGoogle Scholar
  27. Mehta T, Coppi MV, Childers SE, Lovley DR (2005) Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl Environ Microbiol 71(12):8634–8641CrossRefPubMedPubMedCentralGoogle Scholar
  28. Mock J, Wang S, Huang H, Kahnt J, Thauer RK (2014) Evidence for a hexaheteromeric methylenetetrahydrofolate reductase in Moorella thermoacetica. J Bacteriol 196(18):3303–3314CrossRefPubMedPubMedCentralGoogle Scholar
  29. Nevin KP, Hensley SA, Franks AE, Summers ZM, Ou J, Woodard TL, Snoeyenbos-West OL, Lovley DR (2011) Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl Environ Microbiol 77(9):2882–2886CrossRefPubMedPubMedCentralGoogle Scholar
  30. Nevin KP, Woodard TL, Franks AE, Summers ZM, Lovley DR (2010) Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. mBio 1(2):e00103–10Google Scholar
  31. Nie H, Zhang T, Cui M, Lu H, Lovley DR, Russell TP (2013) Improved cathode for high efficient microbial-catalyzed reduction in microbial electrosynthesis cells. Phys Chem Chem Phys 15(34):14290–14294CrossRefPubMedGoogle Scholar
  32. Nybo SE, Khan NE, Woolston BM, Curtis WR (2015) Metabolic engineering in chemolithoautotrophic hosts for the production of fuels and chemicals. Metab Eng 30:105–120CrossRefPubMedGoogle Scholar
  33. Pierce E, Xie G, Barabote RD, Saunders E, Han CS, Detter JC, Richardson P, Brettin TS, Das A, Ljungdahl LG, Ragsdale SW (2008) The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum). Environ Microbiol 10(10):2550–2573CrossRefPubMedPubMedCentralGoogle Scholar
  34. Pohlmann A, Fricke WF, Reinecke F, Kusian B, Liesegang H, Cramm R, Eitinger T, Ewering C, Pötter M, Schwartz E, Strittmatter A, Voss I, Gottschalk G, Steinbüchel A, Friedrich B, Bowien B (2006) Genome sequence of the bioplastic-producing “Knallgas” bacterium Ralstonia eutropha H16. Nat Biotechnol 24(10):1257–1262CrossRefPubMedGoogle Scholar
  35. Potter MC (1911) Electrical effects accompanying the decomposition of organic compounds. Proc R Soc Lond B Biol Sci 84(571):260–276CrossRefGoogle Scholar
  36. Rabaey K, Rozendal RA (2010) Microbial electrosynthesis – revisiting the electrical route for microbial production. Nat Rev Microbiol 8(10):706–716CrossRefPubMedGoogle Scholar
  37. Ragsdale SW (2008) Enzymology of the wood-Ljungdahl pathway of acetogenesis. Ann N Y Acad Sci 1125:129–136CrossRefPubMedPubMedCentralGoogle Scholar
  38. Reece SY, Hamel JA, Sung K, Jarvi TD, Esswein AJ, Pijpers JJH, Nocera DG (2011) Wireless solar water splitting using silicon-based semiconductors and earth-abundant catalysts. Science 334(6056):645–648CrossRefPubMedGoogle Scholar
  39. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435(7045):1098–1101CrossRefPubMedGoogle Scholar
  40. Richter H, Nevin KP, Jia H, Lowy DA, Lovley DR, Tender LM (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. Energ Environ Sci 2(5):506CrossRefGoogle Scholar
  41. Ross DE, Flynn JM, Baron DB, Gralnick JA, Bond DR (2011) Towards electrosynthesis in shewanella: energetics of reversing the mtr pathway for reductive metabolism. PLoS One 6(2):e16649CrossRefPubMedPubMedCentralGoogle Scholar
  42. Sakimoto KK, Wong AB, Yang P (2015) Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351(6268):74–77CrossRefGoogle Scholar
  43. Sakimoto KK, Zhang SJ, Yang P (2016) Cysteine-cystine photoregeneration for oxygenic photosynthesis of acetic acid from CO2 by a tandem inorganic-biological hybrid system. Nano Lett. doi:10.1021/acs.nanolett.6b02740PubMedGoogle Scholar
  44. Schuchmann K, Müller V (2014) Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12(12):809–821CrossRefPubMedGoogle Scholar
  45. Schuster E, Schlegel HG (1967) Chemolithotrophic growth of hydrogenomonas H16 using electrolytic production of hydrogen and oxygen in a chemostat. Arch Microbiol 58(4):380–409Google Scholar
  46. Shi L, Richardson DJ, Wang Z, Kerisit SN, Rosso KM, Zachara JM, Fredrickson JK (2009) The roles of outer membrane cytochromes of Shewanella and Geobacter in extracellular electron transfer. Environ Microbiol Rep 1(4):220–227CrossRefPubMedGoogle Scholar
  47. Strycharz SM, Glaven RH, Coppi MV, Gannon SM, Perpetua LA, Liu A, Nevin KP, Lovley DR (2011) Gene expression and deletion analysis of mechanisms for electron transfer from electrodes to Geobacter sulfurreducens. Bioelectrochemistry 80(2):142–150CrossRefPubMedGoogle Scholar
  48. Torella JP, Gagliardi CJ, Chen JS, Bediako DK, Colón B, Way JC, Silver PA, Nocera DG (2015) Efficient solar-to-fuels production from a hybrid microbial-water-splitting catalyst system. Proc Natl Acad Sci U S A 112(8):2337–2342CrossRefPubMedPubMedCentralGoogle Scholar
  49. Tremblay P-L, Zhang T (2015) Electrifying microbes for the production of chemicals. Front Microbiol 6:201PubMedPubMedCentralGoogle Scholar
  50. Tremblay P-L, Zhang T, Dar SA, Leang C, Lovley DR (2012) The Rnf complex of Clostridium ljungdahlii is a proton-translocating ferredoxin:NAD+ oxidoreductase essential for autotrophic growth. mBio 4(1):e00406–e00412CrossRefPubMedPubMedCentralGoogle Scholar
  51. Wang S, Huang H, Kahnt J, Thauer RK (2013) A reversible electron-bifurcating ferredoxin- and NAD-dependent [FeFe]-hydrogenase (HydABC) in Moorella thermoacetica. J Bacteriol 195(6):1267–1275CrossRefPubMedPubMedCentralGoogle Scholar
  52. Zhang T (2015) More efficient together. Science 350(6262):738–739CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2016

Authors and Affiliations

  • Jongoh Shin
    • 1
  • Yoseb Song
    • 1
  • Sangrak Jin
    • 1
  • Suhyung Cho
    • 1
  • Byung-Kwan Cho
    • 1
  1. 1.Department of Biological ScienceKorea Advanced Institute of Science and Technology (KAIST)DaejeonRepublic of Korea

Personalised recommendations