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Applied Microbiology and Biotechnology

, Volume 101, Issue 16, pp 6301–6307 | Cite as

Extracellular electron transfer in acetogenic bacteria and its application for conversion of carbon dioxide into organic compounds

  • Kensuke Igarashi
  • Souichiro KatoEmail author
Mini-Review

Abstract

Acetogenic bacteria (i.e., acetogens) produce acetate from CO2 during anaerobic chemoautotrophic growth. Because acetogens fix CO2 with high energy efficiency, they have been investigated as biocatalysts of CO2 conversion into valuable chemicals. Recent studies revealed that some acetogens are capable of extracellular electron transfer (EET), which enables electron exchange between microbial cells and extracellular solid materials. Thus, acetogens are promising candidates as biocatalysts in recently developed bioelectrochemical technologies, including microbial electrosynthesis (MES), in which useful chemicals are biologically produced from CO2 using electricity as the energy source. In microbial photoelectrosynthesis, a variant of MES technology, the conversion of CO2 into organic compounds is achieved using light as the sole energy source without an external power supply. In this mini-review, we introduce the general features of bioproduction and EET of acetogens and describe recent progress and future prospects of MES technologies based on the EET capability of acetogens.

Keywords

acetogen CO2fixation bioproduction extracellular electron transfer microbial electrosynthsis 

Notes

Acknowledgments

This work was financially supported by the Japan Society for the Promotion of Science KAKENHI grants (nos. JP16K14895 and JP15H01071).

Compliance with ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abubackar HN, Veiga MC, Kennes C (2015) Carbon monoxide fermentation to ethanol by Clostridium autoethanogenum in a bioreactor with no accumulation of acetic acid. Bioresour Technol 186:122–127CrossRefPubMedGoogle Scholar
  2. Alper H, Stephanopoulos G (2009) Engineering for biofuels: exploiting innate microbial capacity or importing biosynthetic potential? Nat Rev Microbiol 7:715–723CrossRefPubMedGoogle Scholar
  3. Bajracharya S, Vanbroekhoven K, Buisman CJN, Pant D, Strik DPBTB (2016) Application of gas diffusion biocathode in microbial electrosynthesis from carbon dioxide. Environ Sci Pollut Res Int 23:22292–22308CrossRefPubMedGoogle Scholar
  4. Banerjee A, Leang C, Ueki T, Nevin KP, Lovley DR (2014) Lactose-inducible system for metabolic engineering of Clostridium ljungdahlii. Appl Environ Microbiol 80:2410–2416CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bar-Even A, Noor E, Milo R (2012) A survey of carbon fixation pathways through a quantitative lens. J Exp Bot 63:2325–2342CrossRefPubMedGoogle Scholar
  6. Berg IA, Kockelkorn D, Ramos-Vera WH, Say SF, Zarzycki J, Hugler M, Alber BE, Fuchs G (2010) Autotrophic carbon fixation in archaea. Nat Rev Microbiol 8:447–460CrossRefPubMedGoogle Scholar
  7. de Campos RT, Rosenbaum MA (2014) Microbial electroreduction: screening for new cathodic biocatalysts. ChemElectroChem 1:1916–1922CrossRefGoogle Scholar
  8. Chen L, Tremblay P-L, Mohanty S, Xu K, Zhang T (2016) Electrosynthesis of acetate from CO2 by a highly structured biofilm assembled with reduced graphene oxide-tetraethylene pentamine. J Mater Chem A 4:8395–8401CrossRefGoogle Scholar
  9. Choi O, Sang BI (2016) Extracellular electron transfer from cathode to microbes: application for biofuel production. Biotechnol Biofuels 9:11CrossRefPubMedPubMedCentralGoogle Scholar
  10. Coman V, Gustavsson T, Finkelsteinas A, von Wachenfeldt C, Hägerhäll C, Gorton L (2009) Electrical wiring of live, metabolically enhanced Bacillus subtilis cells with flexible osmium-redox polymers. J Am Chem Soc 131:16171–16176CrossRefPubMedGoogle Scholar
  11. Daniell J, Kӧpke M, Simpson SD (2012) Commercial biomass syngas fermentation. Energies 5:5372–5417CrossRefGoogle Scholar
  12. Deutzmann JS, Sahin M, Spormann AM (2015) Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis. MBio 6:e00496-15CrossRefPubMedPubMedCentralGoogle Scholar
  13. Drake HL, Gössner AS, Daniel SL (2008) Old acetogens, new light. Ann N Y Acad Sci 1125:100–128CrossRefPubMedGoogle Scholar
  14. Dürre P, Eikmanns BJ (2015) C1-carbon sources for chemical and fuel production by microbial gas fermentation. Curr Opin Biotechnol 35:63–72CrossRefPubMedGoogle Scholar
  15. Fuchs G (2011) Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? Annu Rev Microbiol 65:631–658CrossRefPubMedGoogle Scholar
  16. Ganigué R, Puig S, Batlle-Vilanova P, Balaguer MD, Colprim J (2015) Microbial electrosynthesis of butyrate from carbon dioxide. Chem Commun 51:3235–3238CrossRefGoogle Scholar
  17. Genthner BRS, Bryant MP (1982) Growth of Eubacterium limosum with carbon monoxide as the energy source. Appl Environ Microbiol 43:70–74PubMedPubMedCentralGoogle Scholar
  18. Giddings CG, Nevin KP, Woodward T, Lovley DR, Butler CS (2015) Simplifying microbial electrosynthesis reactor design. Front Microbiol 6:468CrossRefPubMedPubMedCentralGoogle Scholar
  19. Gong Y, Ebrahim A, Feist AM, Embree M, Zhang T, Lovley D, Zengler K (2013) Sulfide-driven microbial electrosynthesis. Environ Sci Technol 47:568–573CrossRefPubMedGoogle Scholar
  20. Hongo M, Iwahara M (1979) Electrochemical studies on fermentation. I. Application of electro-energizing method to L-glutamic acid fermentation. Agric Biol Chem 43:2075–2081Google Scholar
  21. Jeon BY, Jung IL, Park DH (2012) Conversion of carbon dioxide to metabolites by Clostridium acetobutylicum KCTC1037 cultivated with electrochemical reducing power. Adv Microbiol 2:332–339CrossRefGoogle Scholar
  22. Jourdin L, Lu Y, Flexer V, Keller J, Freguia S (2016) Biologically-induced hydrogen production drives high rate / high efficiency microbial electrosynthesis of acetate from carbon dioxide. ChemElectroChem 3:581–591CrossRefGoogle Scholar
  23. Kaneko M, Ishikawa M, Song J, Kato S, Hashimoto K, Nakanishi S (2017) Cathodic supply of electrons to living microbial cells via cytocompatible redox-active polymers. Electrochem Commun 75:17–20CrossRefGoogle Scholar
  24. Kato S (2015) Biotechnological aspects of microbial extracellular electron transfer. Microbes Environ 30:133–139CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kato S (2016) Microbial extracellular electron transfer and its relevance to iron corrosion. Microb Biotechnol 9:141–148CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kato S, Yumoto I, Kamagata Y (2015) Isolation of acetogenic bacteria that induce biocorrosion by utilizing metallic iron as the sole electron donor. Appl Environ Microbiol 81:67–73CrossRefPubMedGoogle Scholar
  27. Kim TS, Kim BH (1988) Electron flow shift in Clostridium acetobutylicum fermentation by electrochemically introduced reducing equivalent. Biotechnol Lett 10:123–128CrossRefGoogle Scholar
  28. Klasson KT, Ackerson MD, Clausen EC, Gaddy JL (1992) Bioconversion of synthesis gas into liquid or gaseous fuels. Enzym Microb Technol 14:602–608CrossRefGoogle Scholar
  29. 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 107:13087–13092CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kornienko N, Sakimoto KK, Herlihy DM, Nguyen SC, Alivisatos AP, Harris CB, Schwartzberg A, Yang P (2016) Spectroscopic elucidation of energy transfer in hybrid inorganic-biological organisms for solar-to-chemical production. Proc Natl Acad Sci U S A 113:11750–11755CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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 79:1102–1109CrossRefPubMedPubMedCentralGoogle Scholar
  32. Li H, Opgenorth PH, Wernick DG, Rogers S, Wu TY, Higashide W, Malati P, Huo YX, Cho KM, Liao JC (2012) Integrated electromicrobial conversion of CO2 to higher alcohols. Science 335:1596CrossRefPubMedGoogle Scholar
  33. Liew F, Martin ME, Tappel RC, Heijstra BD, Mihalcea C, Köpke M (2016) Gas fermentation—a flexible platform for commercial scale production of low-carbon-fuels and chemicals from waste and renewable feedstocks. Front Microbiol 7:694CrossRefPubMedPubMedCentralGoogle Scholar
  34. Liu C, Gallagher JJ, Sakimoto KK, Nichols EM, Chang CJ, Chang MCY, Yang P (2015) Nanowire-bacteria hybrids for unassisted solar carbon dioxide fixation to value-added chemicals. Nano Lett 15:3634–3639CrossRefPubMedGoogle Scholar
  35. Liu C, Colón BC, Ziesack M, Silver PA, Nocera DG (2016) Water splitting-biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis. Science 352:1210–1213CrossRefPubMedGoogle Scholar
  36. Ljungdahl LG (2009) A life with acetogens, thermophiles, and cellulolytic anaerobes. Annu Rev Microbiol 63:1–25CrossRefPubMedGoogle Scholar
  37. Logan BE (2010) Scaling up microbial fuel cells and other bioelectrochemical systems. Appl Microbiol Biotechnol 85:1665–1671CrossRefPubMedGoogle Scholar
  38. Lovley DR, Nevin KP (2013) Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity. Curr Opin Biotechnol 24:385–390CrossRefPubMedGoogle Scholar
  39. Lu A, Li Y, Jin S, Wang X, Wu XL, Zeng C, Li Y, Ding H, Hao R, Lv M, Wang C, Tang Y, Dong H (2012) Growth of non-phototrophic microorganisms using solar energy through mineral photocatalysis. Nat Commun 3:768CrossRefPubMedGoogle Scholar
  40. Mand J, Park HS, Jack TR, Voordouw G (2014) The role of acetogens in microbially influenced corrosion of steel. Front Microbiol 5:268CrossRefPubMedPubMedCentralGoogle Scholar
  41. Marshall CW, Ross DE, Fichot EB, Norman RS, May HD (2012) Electrosynthesis of commodity chemicals by an autotrophic microbial community. Appl Environ Microbiol 78:8412–8420CrossRefPubMedPubMedCentralGoogle Scholar
  42. Marshall CW, Ross DE, Fichot EB, Norman RS, May HD (2013) Long-term operation of microbial electrosynthesis systems improves acetate production by autotrophic microbiomes. Environ Sci Technol 47:6023–6029CrossRefPubMedGoogle Scholar
  43. 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 105:3968–3973CrossRefPubMedPubMedCentralGoogle Scholar
  44. May HD, Evans PJ, LaBelle EV (2016) The bioelectrosynthesis of acetate. Curr Opin Biotechnol 42:225–233CrossRefPubMedGoogle Scholar
  45. Mohanakrishna G, Seelam JS, Vanbroekhoven K, Pant D (2015) An enriched electroactive homoacetogenic biocathode for the microbial electrosynthesis of acetate through carbon dioxide reduction. Faraday Discuss 183:445–462CrossRefPubMedGoogle Scholar
  46. Nagaraju S, Davies NK, Walker DJ, Köpke M, Simpson SD (2016) Genome editing of Clostridium autoethanogenum using CRISPR/Cas9. Biotechnol Biofuels 9:219CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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:e00103-10CrossRefPubMedPubMedCentralGoogle Scholar
  48. 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 77:2882–2886CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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 15:14290–14294CrossRefPubMedGoogle Scholar
  50. Nishio K, Nakamura R, Lin X, Konno T, Ishihara K, Nakanishi S, Hashimoto K (2013) Extracellular electron transfer across bacterial cell membranes via a cytocompatible redox-active polymer. Chem Phys Chem 14:2159–2163CrossRefPubMedGoogle Scholar
  51. 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
  52. Peguin S, Delorme P, Goma G, Soucaille P (1994) Enhanced alcohol yields in batch cultures of Clostridium acetobutylicum using a three-electrode potentiometric system with methyl viologen as electron carrier. Biotechnol Lett 16:269–274CrossRefGoogle Scholar
  53. Pirbadian S, Barchinger SE, Leung KM, Byun HS, Jangir Y, Bouhenni RA, Reed SB, Romine MF, Saffarini DA, Shi L, Gorby YA, Golbeck JH, El-Naggar MY (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 111:12883–12888CrossRefPubMedPubMedCentralGoogle Scholar
  54. Rabaey K, Rozendal RA (2010) Microbial electrosynthesis - revisiting the electrical route for microbial production. Nat Rev Microbiol 8:706–716CrossRefPubMedGoogle Scholar
  55. Rabaey K, Boon N, Siciliano SD, Verhaege M, Verstraete W (2004) Biofuel cells select for microbial consortia that self-mediate electron transfer. Appl Environ Microbiol 70:5373–5382CrossRefPubMedPubMedCentralGoogle Scholar
  56. Ramió-Pujol S, Ganiguẽ R, Bañeras L, Colprim J (2015) Incubation at 25 °C prevents acid crash and enhances alcohol production in Clostridium carboxidivorans P7. Bioresour Technol 192:296–303CrossRefPubMedGoogle Scholar
  57. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101CrossRefPubMedGoogle Scholar
  58. Richter K, Schicklberger M, Gescher J (2012) Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Appl Environ Microbiol 78:913–921CrossRefPubMedPubMedCentralGoogle Scholar
  59. Roger I, Shipman MA, Symes MD (2017) Earth-abundant catalysts for electrochemical and photoelectrochemical water splitting. Nat Rev Chem 1:0003CrossRefGoogle Scholar
  60. Rosenbaum MA, Henrich AW (2014) Engineering microbial electrocatalysis for chemical and fuel production. Curr Opin Biotechnol 29:93–98CrossRefPubMedGoogle Scholar
  61. Rosenbaum M, Aulenta F, Villano M, Angenent LT (2011) Cathodes as electron donors for microbial metabolism: which extracellular electron transfer mechanisms are involved? Bioresour Technol 102:324–333CrossRefPubMedGoogle Scholar
  62. Sakimoto KK, Wong AB, Yang P (2016a) Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351:74–77CrossRefPubMedGoogle Scholar
  63. Sakimoto KK, Zhang SJ, Yang P (2016b) Cysteine-cystine photoregeneration for oxygenic photosynthesis of acetic acid from CO2 by a tandem inorganic-biological hybrid system. Nano Lett 16:5883–5887CrossRefPubMedGoogle Scholar
  64. Schiel-Bengelsdorf B, Dürre P (2012) Pathway engineering and synthetic biology using acetogens. FEBS Lett 586:2191–2198CrossRefPubMedGoogle Scholar
  65. Shi L, Dong H, Reguera G, Beyenal H, Lu A, Liu J, Yu HQ, Fredrickson JK (2016) Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol 14:651–662CrossRefPubMedGoogle Scholar
  66. Song J, Kim Y, Lim M, Lee H, Lee JI, Shin W (2011) Microbes as electrochemical CO2 conversion catalysts. ChemSusChem 4:587–590CrossRefPubMedGoogle Scholar
  67. Steinbusch KJ, Hamelers HVM, Plugge CM, Buisman CJN (2011) Biological formation of caproate and caprylate from acetate: fuel and chemicals from low grade biomass. Energy Environ Sci 4:216–224CrossRefGoogle Scholar
  68. Thrash JC, Coates JD (2008) Review: direct and indirect electrical stimulation of microbial metabolism. Environ Sci Technol 42:3921–3931CrossRefPubMedGoogle Scholar
  69. 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 112:2337–2342CrossRefPubMedPubMedCentralGoogle Scholar
  70. Tremblay PL, Zhang T (2015) Electrifying microbes for the production of chemicals. Front Microbiol 6:201PubMedPubMedCentralGoogle Scholar
  71. Tremblay PL, Höglund D, Koza A, Bonde I, Zhang T (2015) Adaptation of the autotrophic acetogen Sporomusa ovata to methanol accelerates the conversion of CO2 to organic products. Sci Rep 5:16168CrossRefPubMedPubMedCentralGoogle Scholar
  72. Tremblay PL, Angenent LT, Zhang T (2016) Extracellular electron uptake: among autotrophs and mediated by surfaces. Trends Biotechnol 35:360–371CrossRefPubMedGoogle Scholar
  73. Ueki T, Nevin KP, Woodard TL, Lovley DR (2014) Converting carbon dioxide to butyrate with an engineered strain of Clostridium ljungdahlii. MBio 5:e01636-14CrossRefPubMedPubMedCentralGoogle Scholar
  74. Van Eerten-Jansen MCAA, Ter Heijne A, Grootscholten TIM, Steinbusch KJJ, Sleutels THJA, Hamelers HVM, Buisman CJN (2013) Bioelectrochemical production of caproate and caprylate from acetate by mixed cultures. ACS Sustain Chem Eng 1:513–518CrossRefGoogle Scholar
  75. Varcoe JR, Atanassov P, Dekel DR, Herring AM, Hickner MA, Kohl PA, Kucernak AR, Mustain WE, Nijmeijer K, Scott K, Xu T, Zhuang L (2014) Anion-exchange membranes in electrochemical energy systems. Energy Environ Sci 7:3135–3191CrossRefGoogle Scholar
  76. Watanabe K, Manefield M, Lee M, Kouzuma A (2009) Electron shuttles in biotechnology. Curr Opin Biotechnol 20:633–641CrossRefPubMedGoogle Scholar
  77. Zhang T, Nie H, Bain TS, Lu H, Cui M, Snoeyenbos-West OL, Franks AE, Nevin KP, Russell TP, Lovley DR (2013) Improved cathode materials for microbial electrosynthesis. Energy Environ Sci 6:217–224CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST)SapporoJapan
  2. 2.Division of Applied Bioscience, Graduate School of AgricultureHokkaido UniversitySapporoJapan

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